Plant nutrients can be recycled through microbial
decomposition of organic matter but replacement of base cations and
phosphorus, lost through harvesting of biomass/biofuels or leaching,
requires de novo supply of fresh nutrients released through weathering of soil
parent material (minerals and rocks). Weathering involves physical and
chemical processes that are modified by biological activity of plants,
microorganisms and animals. This article reviews recent progress made in
understanding biological processes contributing to weathering. A perspective
of increasing spatial scale is adopted, examining the consequences of
biological activity for weathering from nanoscale interactions, through in vitro and
in planta microcosm and mesocosm studies, to field experiments, and finally ecosystem
and global level effects. The topics discussed include the physical
alteration of minerals and mineral surfaces; the composition, amounts,
chemical properties, and effects of plant and microbial secretions; and the
role of carbon flow (including stabilisation and sequestration of C in organic
and inorganic forms). Although the predominant focus is on the effects of
fungi in forest ecosystems, the properties of biofilms, including bacterial
interactions, are also discussed. The implications of these biological
processes for modelling are discussed, and we attempt to identify some key
questions and knowledge gaps, as well as experimental approaches and areas
of research in which future studies are likely to yield useful results. A
particular focus of this article is to improve the representation of the
ways in which biological processes complement physical and chemical
processes that mobilise mineral elements, making them available for plant
uptake. This is necessary to produce better estimates of weathering that are
required for sustainable management of forests in a post-fossil-fuel
economy. While there are abundant examples of nanometre- and micrometre-scale
physical interactions between microorganisms and different minerals, opinion
appears to be divided with respect to the quantitative significance of these
observations for overall weathering. Numerous in vitro experiments and microcosm
studies involving plants and their associated microorganisms suggest that
the allocation of plant-derived carbon, mineral dissolution and plant
nutrient status are tightly coupled, but there is still disagreement about
the extent to which these processes contribute to field-scale observations.
Apart from providing dynamically responsive pathways for the allocation of
plant-derived carbon to power dissolution of minerals, mycorrhizal mycelia
provide conduits for the long-distance transportation of weathering products
back to plants that are also quantitatively significant sinks for released
nutrients. These mycelial pathways bridge heterogeneous substrates, reducing
the influence of local variation in C:N ratios. The production of
polysaccharide matrices by biofilms of interacting bacteria and/or fungi at
interfaces with mineral surfaces and roots influences patterns of
production of antibiotics and quorum sensing molecules, with concomitant
effects on microbial community structure, and the qualitative and
quantitative composition of mineral-solubilising compounds and weathering
products. Patterns of carbon allocation and nutrient mobilisation from both
organic and inorganic substrates have been studied at larger spatial and
temporal scales, including both ecosystem and global levels, and there is a
generally wider degree of acceptance of the “systemic” effects of
microorganisms on patterns of nutrient mobilisation. Theories about the
evolutionary development of weathering processes have been advanced but
there is still a lack of information connecting processes at different
spatial scales. Detailed studies of the liquid chemistry of local weathering
sites at the micrometre scale, together with upscaling to soil-scale
dissolution rates, are advocated, as well as new approaches involving stable
isotopes.
Introduction
Modelling of base cation supply using the PROFILE/ForSAFE modelling platform
(Kronnäs et al., 2019) suggests that planned intensification of Swedish
forestry, involving increased harvesting of organic residues for biofuel,
will not be sustainable in the long term without compensatory
measures such as wood ash recycling (Akselsson et al., 2007; Klaminder et
al., 2011; Futter et al., 2012; Moldan et al., 2017). The base cations and
phosphorus that are essential for forest growth can be recycled from
organic residues through microbial decomposition. However, if they are lost
through removal of organic material, the only way they can be replaced is by
weathering of rocks and minerals, or deposition from the atmosphere. There
is a need to improve the available estimates of weathering and to improve
our knowledge of the ways in which biological processes may complement
physical and chemical processes that mobilise mineral elements, making them
available for plant uptake.
The role of fungi in biological weathering in boreal forest soils was
reviewed by Hoffland et al. (2004) and by Finlay et al. (2009). More
recent reviews of the more specific roles of mycorrhizal symbiosis in
mineral weathering and nutrient mining from soil parent material (Smits and
Wallander, 2017), pedogenesis (Leake and Read, 2017) and immobilisation of
carbon in mycorrhizal mycelial biomass and secretions (Finlay and
Clemmensen, 2017) have also been published. Twelve testable hypotheses on
the geobiology of weathering were outlined by Brantley et al. (2011). These
authors concede that some of the outlined hypotheses have been implicit in
scientific research conducted since the late 1800s but argue that there are
now new analytical, modelling and field opportunities to test these
hypotheses. The aim of the present article is to review recent advances in
the understanding of biological weathering, particularly with respect to
nutrient and carbon cycling within boreal forests, including findings made
within the interdisciplinary project Quantifying Weathering Rates for Sustainable Forestry (QWARTS, 2012–2016). One major
motivation for this study was the concern that the modelling tools used to
determine the long-term supply of weathering products for sustainable forest
growth may have been missing biological processes that allow a forest
ecosystem to alter the rate of weathering in response to the biological
demand for these weathering products (Klaminder et al., 2011).
Biological weathering involves the weakening and disintegration of rocks and
dissolution of minerals, caused by the activity of plants, animals and
microorganisms. Biological weathering takes place in conjunction with
physical and chemical processes, but there is still disagreement about the
quantitative contribution of biogenic weathering to overall weathering (see
Leake and Read, 2017; Smits and Wallander, 2017). The first of the 12 hypotheses of Brantley et
al. (2011) is that “Solar-to-chemical conversion of energy by plants regulates flows of carbon, water, and nutrients through plant-microbe soil networks, thereby controlling the location and extent of biological weathering”. The supply and transport of
photosynthetically derived carbon through roots and mycorrhizal hyphae to
organic and inorganic substrates is a fundamental biogeochemical process
(Jones et al., 2009), influencing both decomposition and mineral weathering,
and these two processes influence each other. This flow of carbon and the
role of plant–microbe–soil interactions in the rhizosphere have been
reviewed from an evolutionary perspective (Lambers et al., 2009) and with
respect to their potential applications in sustainable agriculture, nature
conservation, the development of bioenergy crops and the mitigation of
climate change (Philippot et al., 2013). Since there is disagreement about
whether biological processes demonstrated at small spatial scales contribute
significantly to field-scale processes but a greater degree of consensus
about the importance of systemic effects of biological weathering at larger
spatial and temporal scales, we have adopted a spatial perspective. We start
by reviewing processes occurring at the nanometre and micrometre scale before
discussing in vitro microcosm experiments, mesocosm studies with plants, field
experiments, and finally studies of effects at the ecosystem and global
scale. Biological weathering is also discussed from an evolutionary
perspective, and some recent experiments using stable isotopes are presented.
Each section is followed by a short summary in which we attempt to list the
main conclusions and some of the remaining questions and knowledge gaps.
Finally, different modelling approaches are discussed in relation to how we
can incorporate the biological features discussed earlier and improve the
reliability of models.
Microscale–nanoscale observations of physical alteration of minerals
The idea that microorganisms may alter rocks and minerals is not new, and
biogenic etching of microfractures in borosilicate glass and crystalline
silicates (olivine) by microfungi (Penicillium notatum and Aspergillus amstelodami), presumed to be producing both
organic acids and siderophores, was demonstrated by Callot et al. (1987).
Early studies by Paris et al. (1995, 1996) demonstrated in vitro weathering of
phlogopite involving displacement of non-exchangeable interlayer K+ and
alteration of the crystal lattice structure, as well as stimulated
accumulation of oxalate under simultaneous K+ and Mg2+ deficiency.
The widespread occurrence of tubular pores, 3–10 µm in diameter, has
been demonstrated in weatherable minerals in podzol surface soils and
shallow granitic rock under European coniferous forests (van Breemen et
al., 2000; Jongmans et al., 1997; Landeweert et al., 2001). Some of these pores
were found to be occupied by fungal hyphae, and the authors speculated that
they could be formed by the weathering action of hyphae (possibly in
association with bacteria) releasing organic acids and siderophores. The
aetiology of pore formation has been questioned however, with some authors
claiming that (all) the observed pores are of abiotic origin (Sverdrup,
2009). Studies of feldspar tunnelling along chronosequences created by
postglacial rebound (Hoffland et al., 2002) revealed that the tunnels were
more frequent in the uppermost 2 cm of the E horizon, that the frequency of
tunnelling increased with soil age, and that there was a lag period of up to
2000 years when tunnels were absent or rare, postulated by the authors to
coincide with the time taken for the disappearance of the more easily
weatherable K and Ca containing biotite and hornblende. Parallel studies
along productivity gradients (Hoffland et al., 2003) have also revealed a
significant positive correlation between the density of ectomycorrhizal root
tips and the density of tunnels in the E horizon. However similar tunnels in
feldspars across a sand dune chronosequence at Lake Michigan have been
estimated to contribute less than 0.5 % of total mineral weathering (Smits
et al., 2005), suggesting either that fungal weathering is negligible or
that tunnel formation reflects only a small proportion of the total weathering effect of the fungi. The total mineral surface area available for mineral weathering in
most mineral soils is clearly much larger than the internal surface area of
the observed tunnels, and small tunnel-like features were observed in mineral
surfaces by Smits et al. (2005). Different biomechanical mechanisms used by
fungi to penetrate rock have received increasing attention. Ultramicroscopic
and spectroscopic observations of fungus–biotite interfaces during
weathering of biotite flakes have revealed biomechanical forcing and
altered interlayer spacing associated with depletion of K by an
ectomycorrhizal fungus (Paxillus involutus; Bonneville et al., 2009). It appears that
physical distortion of the lattice structure takes place before chemical
alteration through dissolution and oxidation. Fungal hyphae colonising
fractures and voids in minerals can exert substantial mechanical force and
have been demonstrated to build up turgor pressure in excess of 8 MPa that
is sufficient to penetrate Mylar and Kevlar and widen existing cracks in
rocks (Howard et al., 1991). Recent studies of biotite colonisation by P. involutus
(Bonneville et al., 2016) have revealed extensive oxidation of Fe(II) up to
2 µm in depth, and the increase in Fe(III) implies a volumetric change
that is sufficient to strain the crystal lattice and induce the formation of
microcracks, which are abundant below the hypha–biotite interface.
The observations of Jongmans et al. (1997) stimulated interest in biogenic
weathering and led to a large number of subsequent studies. The endolithic
biosignatures of rock-inhabiting microorganisms can be distinguished from
purely abiotic microtunnels (McLoughlin et al., 2010). Biological tubular
microcavities can be distinguished by their shapes, distribution and the
absence of intersections which excludes an origin by chemical dissolution of
pre-existing heterogeneities such as radiation damage trails, gas-escape
structures or fluid inclusion trails. Atomic force microscopy (AFM) and
scanning transmission electron microscopy–energy dispersive X-ray
spectroscopy (STEM–EDX) have been used to demonstrate nanoscale alteration
of surface topography and attachment and deposition of organic biolayers by
fungal hyphae (Bonneville et al., 2011; McMaster, 2012; Gazzè et al.,
2013, 2014; Saccone et al., 2012). More recent studies of lizardite
dissolution by fungal cells, using confocal laser scanning microscopy (CLSM)
(Li et al., 2016), suggest that biomechanical forces of hyphal growth are
indispensable for fungal weathering and strong enough to breach the mineral
lattice. The data from these studies suggest that biomechanical forcing
takes place with micrometre-scale acidification mediated by surface-bound
hyphae and subsequent removal of chemical elements due to fungal action.
However, so far, the quantitative significance of these effects for total
weathering rates is still unclear. Comparative studies of forests with
either ectomycorrhizal or arbuscular mycorrhizal host tree species (Koele et
al., 2014) have revealed the presence of tunnel-like structures in minerals
in both types of forest, suggesting that mineral weathering can be caused by
acidification of the rhizosphere by both types of mycorrhizal fungus and/or
saprotrophic fungi. Investigations of silicate mineral surfaces, buried in
proximity to roots of trees that would normally host arbuscular mycorrhizal
fungi (AMF) and were growing in an arboretum (Quirk et al., 2012, 2014a),
suggest that AMF may also form weathering trenches, although the associated
fungi were not identified in these particular studies. Nanoscale channels in
chlorite flakes colonised by ectomycorrhizal fungi have also been
demonstrated (Gazzè et al., 2012) using AFM and suggested as evidence
that fungal activity, fuelled by plant photosynthate, can enhance mineral
dissolution.
Summary
Many new studies, published during the past 10 years, using AFM, CLSM,
energy dispersive X-ray spectroscopy and vertical scanning interferometry,
have revealed the structural alteration of mineral substrates by fungi. The
endolithic signatures of rock-inhabiting microorganisms can now be
distinguished from structures of abiotic origin but the proportional
contribution of tunnels and voids with respect to total biological
weathering is probably low since their volume and internal surface area are
small in comparison to the total mineral surface area exposed to microbial
contact. The capacity of different vegetation systems, hosting different
types of mycorrhizal symbionts, to cause structural alteration of different
minerals should be investigated in further studies, combined with DNA-based
methods to identify the fungi (and bacteria) involved in situ. The influence of
environmental factors such as atmospheric CO2 concentration, nitrogen
deposition and mineral composition should be investigated.
(a) Schematic diagram showing biofilm structure and
function and the biological and chemical processes that biofilms
influence. (b) Extracellular polymeric substance (EPS)
halos and their possible influence on interactions between hypha
and mineral surfaces (based on observations by Gazzè et
al., 2013). (Figure 1a is reproduced with permission from Flemming et
al., 2016.)
Biofilms and small-scale microbial interactions with consequences at
higher spatial scales
Most microorganisms do not live as pure cultures of dispersed single cells
in soil solution. Instead they aggregate at interfaces – on surfaces of
roots, organic matter, rocks and minerals, forming biofilms or microbial
mats (Flemming and Wingender, 2010; Flemming et al., 2016). Biofilms consist
of a hydrated matrix of extracellular polymeric substances (EPSs), mostly
produced by the organisms they contain. This matrix can account for 90 %
of the dry mass of the biofilm and provides a structural scaffold
responsible for adhesion to surfaces and cohesion of the biofilm, enabling
interactions that are entirely different from those of planktonic bacteria.
The EPS matrix isolates microorganisms from the bulk soil solution,
maintaining them in close proximity to each other and to substrate surfaces,
concentrating weathering agents and allowing cell-to-cell communication and
quorum sensing by containing and concentrating signal molecules. This
permits the formation of synergistic microbial consortia; production,
accumulation, retention and stabilisation of extracellular enzymes through
binding interactions with polysaccharides; sorption of organic compounds and
inorganic ions; redox activity in the matrix (Liu and
Lian, 2019); and horizontal gene transfer (Savage et al., 2013;
Borgeaud et al., 2015). The retention of water maintains a hydrated
microenvironment, protecting against desiccation, and proteins and
polysaccharides can provide a protective barrier against specific and
non-specific host defences during infection, antimicrobial agents and some
grazing protozoa (Fig. 1a) (Flemming and Wingender, 2010).
Biofilms and microbial mats have been studied from different perspectives
that are relevant to interactions between microorganisms and minerals in a
biogeochemical context. Subaerial biofilms occur within solid mineral
surfaces exposed to the atmosphere and are dominated by fungi, algae,
cyanobacteria and heterotrophic bacteria (Gorbushina, 2007). These
communities are known to penetrate the mineral substrates and induce
chemical and physical changes contributing to weathering. Effects of
biofilms containing the phototrophic cyanobacterium Nostoc punctiforme and the rock-inhabiting
ascomycete Knufia petricola have been quantified using inductively coupled plasma optical
emission spectrometry–mass spectrometry as well as scanning electron
microscopy–transmission electron microscopy—energy dispersive X-ray
spectrometry (Seiffert et al., 2014), demonstrating clear effects of the
biofilms on mineral dissolution and leaching. Mats of hypogeous
ectomycorrhizal fungi have been studied by Griffiths et al. (1994), who found
that colonisation by Gautieria monticola notably increased the amount of oxalic acid in soil.
Calcium oxalate (CaOx) can accumulate in forest soils, and deposition of Ca
from the weathering of apatite as CaOx crystals on the hyphal surfaces of
Rhizopogon sp. growing from Pinus muricata seedlings has been shown in microcosm studies (Wallander
et al., 2002). More CaOx is formed under higher P levels (Tuason and Arocena,
2009). Bulk soil solution concentrations of organic acids are considered to
be too low to have a large effect on mineral dissolution, and modelling
(Smits, 2009) suggests that local concentrations of weathering agents such
as oxalate will not have a major effect on feldspar weathering unless the
weathering agents remain within a few microns of the mineral surface.
However, several authors (Balogh-Brunstad et al., 2008; Finlay et al., 2009)
have suggested that higher concentrations of organic acids may accumulate
within EPS matrices that are in close proximity to mineral surfaces, so that
mineral dissolution is influenced, and have called for more experiments to
confirm this possible effect. More recent studies by Gazzè et al. (2013)
using atomic force microscopy have demonstrated the presence of EPS halos
(Fig. 1b) surrounding Paxillus involutus hyphae colonising phyllosilicate surfaces. In
addition to increasing the surface area for hyphal interaction with mineral
surfaces, these hydrated EPS layers presumably enhance mineral weathering by
promoting accumulation of weathering agents such as organic acids and acidic
polysaccharides, but further detailed studies of the local concentrations of
these molecules are still necessary.
Fungi and bacteria live together in a wide range of environments (Deveau et
al., 2018), and the exudation of carbon compounds from roots and fungal
hyphae into biofilms undoubtedly influences bacterial growth and activity
(Guennoc et al., 2018). Priming of bacterial activity may occur through
supply of exudates from vital hyphae (Toljander et al., 2007) but may also
include recycling of C from damaged or senescing hyphae. Carbon supply from
arbuscular mycorrhizal hyphae can provide energy for associated bacteria to
solubilise phosphate (Zhang et al., 2014, 2016). Different ectomycorrhizal
fungi colonising lateral roots of tree seedlings have been shown to
influence the community structure of associated bacteria (Marupakula et al.,
2016, 2017), and differences in the richness and composition of bacterial
communities have been demonstrated between the hyphosphere of
ectomycorrhizal fungi and that of saprotrophic fungi (Liu et al., 2018).
Although the role of bacteria in mineral weathering has been less widely
studied than that of fungi in recent years, progress has been made in
understanding the identity and mechanisms of bacteria involved in weathering
of minerals in acidic forest soils. Bacteria in the genera Burkholderia and Collimonas appear to
have significant mineral weathering ability (Uroz et al., 2011), and
incubation of different minerals in forest soils appears to result in
selection of different bacterial communities, which are distinct from those
of the bulk soil (Uroz et al., 2012), confirming the concept of
mineralogical control of fungal and bacterial community structure (Gleeson
et al., 2005; Hutchens, 2010). Uroz et al. (2015) contrasted the rhizosphere
with the “mineralosphere” in which bacteria are selected, not by organic
nutrients originating from roots, but by the physiochemical properties of
different minerals. Microorganisms can also drive weathering of bedrock in
subglacial environments, and the ubiquitous nature of pyrite in many common
bedrock types and high SO42- concentrations in most glacial
meltwater have been interpreted to suggest (Mitchell et al., 2013) that
pyrite may be a dominant lithogenic control on subglacial microbial
communities and that mineral-based energy may therefore serve a fundamental
role in sustaining these microbial populations over glacial–interglacial
timescales. Studies by Montross et al. (2013) demonstrated an up to
8-fold increase in dissolved cations in biotic systems containing
glacial sediments and meltwater compared with abiotic systems, suggesting
that microbial processes can maintain terrestrial chemical weathering rates
in cooling climates during glacial advance. Recent experiments attempting to
investigate in situ mineral dissolution rates and structure and diversity of bacterial
communities colonising silicate minerals (Wild et al., 2018, 2019) have
revealed development of mineral-specific bacterial communities and large
discrepancies between predicted and measured dissolution rates, which were
attributed to “heterogeneity of fluid circulation and local variation in
reaction conditions”.
Summary
Consequences of the ecophysiological heterogeneity and spatial organisation
of plant–microbe–soil interactions in natural environments need to be
incorporated into new models and experimental systems. The effects of
biofilms at microbial–mineral interfaces include EPS haloes that increase
the surface area of contact, increased concentrations of weathering agents
through protection by antibiotic compounds secreted into the EPS matrix,
rapid removal of feedback-inhibiting weathering products by mycorrhizal
hyphae attached to plants that act as strong sinks for mobilised products,
and changed patterns of microbial activity due to the facilitation of quorum
sensing and other types of signalling. Retention of water within the biofilm
matrix may allow weathering to be maintained at higher rates than would
otherwise be possible during periods of soil drying. The extremely fine
spatial scale of biofilms necessitates further development of sampling at the
micrometre-scale to capture the steep chemical gradients and micro-scale
variation in chemical and biological diversity and composition. These
measurements are essential in order to gain an accurate picture of the
chemical and biological conditions existing at weathering interfaces.
Microbial and plant secretions – evidence from microcosms and mesocosms
Plants play a fundamental role in soil formation since root activity and
decomposing plant material enhance weathering rates by producing acidifying
substances (H+, organic acids) and ligands that complex with metals in
the minerals. In addition, uptake of ions released from weathering reduces
the likelihood of saturating conditions that retard weathering rates. Many
of these effects are mediated by mycorrhizal fungi, and in temperate and
boreal forests the vast majority of fine tree roots are colonised by
symbiotic ectomycorrhizal fungi.
In ancient, highly weathered soils, P is the primary nutrient limiting plant
growth, whereas N is the main growth-limiting nutrient in young soils. Plant
nutrient acquisition in nutrient-impoverished soils often involves
specialised root structures such as cluster roots or symbiotic structures
such as mycorrhizal associations or root nodules (Lambers et al., 2008). In ancient soils
with very low P availability “dauciform” (carrot-shaped) roots are produced
by monocots in the Cyperaceae, and “proteoid” roots are produced by numerous
dicot families, including the Proteaceae. Both types of roots are hairy and
produce large amounts of carboxylates that desorb P from mineral surfaces.
Phosphatases are also produced to release P from organic sources. Protons
are quantitatively important weathering agents, and many biotic processes,
including uptake of positively charged nutrients such as NH4+ and
K+, result in exudation of protons. Organic acids such as oxalic acid
and citric acid are produced by plant roots as well as fungi and bacteria
and contribute to proton-driven weathering, but their deprotonated forms
also act as strong weathering agents complexing with metals, including
Fe3+ and Al3+ (Ma et al., 2001). Soil P and N change as a function
of soil age, and in younger- and intermediate-aged soils with adequate
amounts of nutrients, mycorrhizal mycelia provide an effective strategy for
nutrient acquisition (Lambers et al., 2008). Experiments using dual isotopic
tracers of 14C and 33P suggest that evolution of land plants
from rootless gametophytes to rooted sporophytes with larger arbuscular
mycorrhizal hyphal networks enabled enhanced efficiency of P capture as
atmospheric CO2 concentrations fell during the mid-Palaeozoic (480–360 Myr ago; Field et al., 2012).
Strategies of mycorrhizal symbiosis differ depending upon the plant host.
The majority of plant species form arbuscular mycorrhizal associations with
Glomeromycotan fungi that are efficient at scavenging nutrients such as P
and transporting it to their plant hosts across the depletion zones around
roots formed by the slow diffusion of P through soil. However, these fungi
are less efficient than proteoid roots at “mining” P and releasing it from
sorbed forms. Ericoid mycorrhizal associations are formed by plants in the Ericaceae,
Empetraceae and Epacridaceae, and ectomycorrhizal associations are formed by many woody
plants and trees (Smith and Read, 2008). The fungi forming these two types
of symbiosis vary in their enzymatic competence, but in general they have a
more highly developed capacity to both scavenge and mine N and P than
arbuscular mycorrhiza, releasing N and P from organic forms (in the case of
ectomycorrhizal fungi) by different combinations of hydrolytic and oxidative
enzymes and non-enzymatic Fenton chemistry (Lindahl and Tunlid, 2015;
Nicolás et al., 2019) and P and other mineral elements from inorganic
forms via proton, organic acid, and siderophore exudation. In boreal forests
with stratified podzol soils, many ectomycorrhizal fungal species produce
extensive fungal mycelia that colonise both organic soil horizons and
mineral horizons to an equal extent on a land area basis
(Söderström, 1979), although data expressed on a soil dry weight
basis often suggest that colonisation of the mineral soil is lower since the
mineral soil has a dry weight approximately 10 times higher than the organic
soil. Studies of vertical distribution of different functional guilds of
fungi (Lindahl et al., 2007; Sterkenburg et al., 2018) suggest that
ectomycorrhizal fungi are more abundant than saprotrophs in deeper organic
and mineral horizons, presumably because they receive supplies of carbon
from their plant hosts and are less reliant on local sources of carbon that
are less abundant in the deeper horizons.
The flow of plant-derived carbon through fungal hyphae to organic and inorganic substrates drives biogeochemical processes such as
decomposition and weathering and influences patterns of C release and sequestration into stable organic and inorganic forms. Carbon is assimilated
by plants (a) and transferred directly to symbiotic mycorrhizal hyphae that transfer nutrients mobilised by the hyphae back to their hosts (b). Products of mycelial respiration are released to the atmosphere (c). The fungal secretome (d) consists of different labile compounds that can
be translocated to different organic or inorganic substrates. These compounds may be released into an extracellular polysaccharide matrix (e) or as droplets that condition the hyphosphere, facilitating interactions with bacteria (f). Hydrolytic and oxidative enzymes (g) mobilise N and P
from plant-derived organic substrates (h) or microbial necromass (i). Peptides and antibiotics play important roles in signalling and influencing
microbiome structure (j), sugars and polyols maintain osmotic gradients and hyphal turgor (k), and low-molecular-weight organic acids and siderophores
influence the mobilisation of P and base cations from minerals (l). Long-term sequestration and stabilisation of carbon can take place
in recalcitrant organic substrates (m) and secondary minerals and mineraloids (n) (reproduced with permission; Finlay and Clemmensen, 2017).
Mycorrhizal fungal mycelia secrete a wide range of molecules and the
secretome has been shown to include low-molecular-weight (LMW) organic
acids, amino acids, polyols, peptides, siderophores, glycoproteins and a
diverse range of enzymes such as proteases, phosphatases, lignin peroxidases
and laccase. The production of these substances is highly variable both
within and between different types of mycorrhizal fungi and influenced by
different environmental conditions. Figure 2 illustrates the flow
of plant-derived carbon compounds through the fungal mycelium, the secretion
of compounds into extracellular polysaccharide matrices and the soil
solution and the longer-term immobilisation processes that result in storage
of stable C in organic and mineral pools. Although many of the molecules
produced by the mycelium and its associated bacteria are labile and subject
to rapid turnover, they play a collective role in mobilisation of nutrients
that can lead to a longer-term sequestration of C in recalcitrant substrates
that are both organic (Clemmensen et al., 2013) and inorganic (Sun et al.,
2019a).
LMW organic acids are frequently identified as important components of the
exudates produced by ectomycorrhizal fungi. Simple carboxylic acids are
often present in soil solution and implicated in pedogenic processes. Their
sorption characteristics were studied by van Hees et al. (2003), who found
adsorbed-to-solution ratios as high as 3100. Organic acids are readily
adsorbed to the solid phase and sorption provides an important buffering
role in maintaining soil solution concentrations at low organic acid
concentrations, inhibiting microbial degradation. Concentrations of LMW
organic compounds in soil solution are typically low (< 50 µM), but the flux through this pool is extremely rapid and microbial
mineralisation to CO2 results in mean residence times of 1–10 h
(van Hees et al., 2005). These labile compounds may thus make a substantial
contribution to the total efflux of CO2 from soil. Direct measurements
of oxalate exudation from hyphal tips of the ectomycorrhizal fungus
Hebeloma crustuliniforme (van Hees et al., 2006) have led to calculated exudation rates of 19±3 fmol oxalate per hyphal tip per hour, suggesting that concentrations of 30 mM oxalate could occur within 1 h inside feldspar tunnels occupied by
fungal hyphae. This would represent a concentration 10 000 times higher than
in the surrounding soil solution. Production of the hydroxamate siderophore
ferricrocin was also detected and calculated to be able to reach a
concentration of 1.5 µM, around 1000 times higher than in the
surrounding soil solution. Interestingly, the steady-state dissolution of
goethite by 2'-deoxymugineic acid (DMA) phytosiderophores has been
demonstrated to be synergistically enhanced by oxalate (Reichard et al.,
2005), and it is possible that synergistic interactions between other
combinations of organic acids and siderophores may exist. Organic acid
production by intact ectomycorrhizal fungal mycelia colonising Pinus sylvestris seedlings
was studied by Ahonen-Jonnarth et al. (2000), using axenic in vitro systems. In this
study, production of oxalic acid by seedlings exposed to elevated (0.7 mM)
Al and colonised by Suillus variegatus or Rhizopogon roseolus was up to 39.5 and 26 times, respectively, higher
than in non-mycorrhizal control plants. The same type of lab system was used
by Johansson et al. (2009) to investigate the effect of different
mycorrhizal fungi on production of LMW organic acids, amino acids and dissolved organic carbon (DOC).
However, in these experiments the identifiable LMW organic acids constituted
only a small proportion (3 %–5 %) of the total DOC fraction, but DOC
production was increased in mycorrhizal treatments relative to the
non-mycorrhizal controls.
Studies of mycorrhizal hyphal exudates using nuclear magnetic resonance (NMR) spectroscopy (Sun et al., 1999)
have revealed exudation of fluid droplets at the hyphal tips of the
ectomycorrhizal fungus Suillus bovinus and found that sugars and polyols comprised 32 %
and peptides 14 % of the exudate mass. Oxalic acids and acetic acid were
also found, and polyols such as mannitol and arabitol are thought to be
important for retaining turgor in fungal hyphae during C translocation along
hydrostatic pressure gradients. High internal pressures in hyphae are
thought to be an evolutionary adaptation to facilitate penetration of both
plant tissues and rock surfaces (Jongmans et al., 1997). This
exudation of droplets may play an important role in conditioning the
immediate environment of hyphal tips, facilitating interactions with
substrates and associated microorganisms, even in drier soils. Similar
observations have been made by Querejeta et al. (2003), who demonstrated that
water obtained by Quercus agrifolia plants, using hydraulic lift, can be transferred to
associated arbuscular mycorrhizal and ectomycorrhizal fungi to maintain
their integrity and activity during drought, even when the fertile upper
soil is dry. Carbon allocation in the form of sugars and polyols (Sun et
al., 1999) may be important in generating turgor pressure in hyphae and has
consequences for weathering of minerals with lattice structure.
While biologically derived molecules such as organic acids and siderophores
are strongly implicated in promoting mineral weathering, it is important to
note that biologically derived ligands may also inhibit mineral weathering.
Among LMW organic acids, only citric and oxalic acids are commonly observed
to stimulate mineral weathering (Neaman et al., 2006; Drever and Stillings,
1997), and humic and fulvic acids, which may dominate dissolved organic
matter in soil solutions, have been observed to exert an inhibitory effect
on mineral dissolution (Ochs, 1996; Drever and Stillings, 1997).
Different microcosm systems have been used to study interactions between
minerals and mycorrhizal fungal mycelia colonising plant seedlings.
Differential allocation of plant-derived C to patches of primary minerals
such as quartz and potassium feldspar (Rosling et al., 2004) and to apatite
and quartz (Smits et al., 2012) suggests tightly coupled plant–fungal
interactions underlying weathering. In the experiment by Smits et al. (2012),
when P was limiting, 17 times more 14C was allocated to wells
containing apatite than to those containing only quartz, and fungal
colonisation of the substrate increased the release of P by a factor of
almost 3. Experiments by van Schöll et al. (2006a)
demonstrated that limitation of nutrients (P, Mg, K) affected the
composition of organic acids exuded by ectomycorrhizal fungi (more oxalate)
but not the total amounts. Other experiments by van Schöll et al. (2006b) have demonstrated significant weathering of muscovite by
the ectomycorrhizal fungus Paxillusinvolutus when K was in low supply whereas no effect on
hornblende was found under Mg deficiency. Selective allocation of biomass to
grains of different minerals by P. involutus has also been demonstrated (Leake et al.,
2008; Smits et al., 2008), suggesting grain-scale “biosensing”; however it
is also possible that fungal growth may be influenced by topographic
structure (Smits and Wallander, 2017). Schmalenberger et al. (2015)
demonstrated mineral-specific exudation of oxalate by P. involutus using labelled
14CO2 given to the host plant. Oxalate was exuded in response to
minerals in the following sequence: Gabbro > limestone, olivine
and basalt > granite and quartz. Experiments using flow-through
systems (Calvaruso et al., 2013) have also estimated weathering rates of
apatite to be 10 times higher when pine seedlings were present, compared
with unplanted systems, and attributed this to exudation of organic acids by
the roots. The plants had been checked for the absence of fungal
“contaminants” but inoculation with the mineral weathering bacterial strain
Burkholderia glathei PML1(12)Rp appeared to have no significant effect on weathering.
Fungi, bacteria and plants all produce siderophores, low-molecular-mass,
metal-complexing compounds. These bind strongly to Fe3+, influencing
its release and uptake (Kraemer et al., 2014; Ahmed and
Holmström, 2014). The hydroxamate siderophores
ferrichrome and ferricrocin have been found in a soil solution of more layer
podzolic soil overlying granitic rock and intensively colonised by
ectomycorrhizal hyphae (Holmström et al., 2004) and should be
kinetically and thermodynamically even more efficient complexing agents for
trivalent cations than oxalic and citric acid. Primary minerals containing
substantial amounts of Fe, such as hornblende and biotite, show enhanced
dissolution rates in the presence of bacterial or fungal siderophores
(Kalinowski et al., 2000; Sokolova et al., 2010), and attachment of
microorganisms to the mineral surfaces appears to lead to greater
dissolution of elements from biotite (Bonneville et al., 2009; Ahmed and
Holmström, 2015).
Release of potassium from K-feldspar and illite in microcosms by the fungus
Aspergillus fumigatus was demonstrated by Lian et al. (2008), who showed that release of K was
enhanced by a factor of 3–4 by physical contact between the fungus and the
mineral surface. Simple types of microcosm are usually used for gene
expression studies in order to facilitate extraction of RNA from target
organisms. Xiao et al. (2012) used differential expression cDNA libraries of
A. fumigatus using suppression subtractive hybridisation technology to investigate the
mechanisms by which the fungus weathered K-bearing minerals. K-bearing
minerals were found to upregulate the expression of carbonic anhydrase (CA),
implying that A. fumigatus was capable of converting CO2 into carbonate to
accelerate the weathering of potassium-bearing minerals, which fixed
CO2. During mineral weathering, the fungus changed its metabolism,
produced more metal-binding proteins and reduced membrane metal transporter
expression, which can modulate ion absorption and disposal and promote acid
production. Wang et al. (2015) used high-throughput RNA sequencing (RNA-seq)
to study the molecular mechanisms of Aspergillus niger involved in weathering of potassium
feldspar. The fungus was cultured with soluble K+ or K-feldspar,
demonstrating differential expression of genes related to synthesis and
transportation of organic acids, polysaccharides and proteins, which was
closely related to release of K+ from the minerals. Regulation of
carbonic anhydrase (CA) gene expression in Bacillus mucilaginosus and the effects of its
expression product in Escherichia coli have been examined by Xiao et al. (2014), who found
that expression of CA genes was upregulated by the addition of calcite to a
Ca2+-deficient medium and that a crude enzyme extract of the
expression product in E. coli promoted calcite dissolution. Real-time fluorescent,
quantitative polymerase chain reaction (PCR) has been used to explore the correlation between CA gene
expression in B. mucilaginosus and deficiency or sufficiency of Ca and CO2 concentration,
and the results suggest that CA gene expression is negatively correlated
with both CO2 concentration and the ease of obtaining soluble calcium
(Xiao et al., 2015). The roles of different CA genes have also been studied
in Aspergillus nidulans using gene deletion, overexpression and bioinformatics (Sun and Lian,
2019), and the results of this study suggest that the CA gene canA is involved in
weathering of silicate minerals and carbonate formation, catalysing CO2 hydration, and that canB is essential for cellular respiration and biosynthesis
in low-CO2 environments. Recent microcosm studies have also used
transcriptome analysis to investigate weathering of K-containing feldspar
and apatite and demonstrated upregulation of high-affinity ion transporter
systems in the ectomycorrhizal fungus Amanita pantherina (Sun et al., 2019b).
Summary
Earlier microcosm demonstrations of selective allocation of carbon to
different minerals by ectomycorrhizal mycelium have now been complemented by
newer studies demonstrating that selective C allocation to nutrient-containing minerals through intact ectomycorrhizal mycelium results in
significant increases in nutrient uptake by the host plants (Smits et al.,
2012). There is still disagreement about the relative importance of
different molecules as weathering agents, and better information is required
about their chemical identity, concentration and rates of turnover at
weathering interfaces. Advances in DNA-based techniques have enabled a range
of microcosm experiments in which the regulation of weathering interactions
between fungi and minerals has been examined in microcosms, and further
studies based on transcriptomics will provide a more detailed understanding
of how weathering of different minerals is regulated in individual species.
However, DNA-based community profiling methods should also be used to
improve understanding of more complex weathering consortia involving both
bacteria and fungi.
Schematic diagram summarising an evolutionary perspective of interactions involving mineral weathering and decomposition. Current rates of mineral weathering
have been influenced by different “events” and processes, including the effects of biological processes on mineral evolution (a), serial endosymbiosis (b) enabling the evolution
of higher plants, and mycorrhizal symbiosis (c) enabling increasing colonisation of substrates by roots and mycorrhizal mycelium (d), leading to more efficient nutrient
uptake and larger amounts of photosynthetic tissue (e). The evolution of ectomycorrhizal fungi (ECM) has enabled efficient extraction of N and P from recalcitrant organic
material (f) powered by higher C allocation and better colonisation of organic and mineral substrates (f, g). Note the timescale of the most recent 500 million years is expanded
by a factor of approximately 8.
Systemic consequences of microorganism–mineral interactions in an
ecological and evolutionary context
There is strong support for the idea that microorganism–mineral interactions
have important consequences at global spatial scales and evolutionary timescales and some of these are illustrated in Fig. 3. Indeed, the concept of
“mineral evolution” (Hazen et al., 2008) suggests that over two-thirds of the number of minerals that exist today (> 5300) are the result of chemical changes mediated by living organisms (Fig. 3a). The
best known of these is the Great Oxidation Event about 2.3 billion years ago
(2.3 Ga) (Kump, 2008; Luo et al., 2016) during which the Earth's atmosphere
changed from one that was almost devoid of oxygen to one that is one-fifth
oxygen. Inclusions of potentially biogenic carbon within Hadean zircons as
old as 4.1 Ga (Bell et al., 2015) suggest that biological processes could
have been operating during the Hadean Eon. Early microbial communities would
have developed within subsurface mineral environments to avoid high levels
of ionising radiation at the interface between the atmosphere and
lithosphere. The subaerial biofilms at this interface today remain
stressful environments (Gorbushina, 2007), but ionising radiation levels are
now much lower due to thickening of the Earth's atmosphere. Biomarker
evidence (Brocks et al., 1999) in rocks formed 200 million years (Myr),
before the increase in atmospheric oxygen, suggests that oxygen was already
being produced before 2.5 Ga. Oxygenic photosynthesis by cyanobacteria is a
likely source of this oxygen but there is evidence that stromatolites were
abundant between 3.4 and 2.4 Ga, prior to the advent of cyanobacteria and
oxygenic photosynthesis (Allen, 2016), and that Archaean microbial mats of
protocyanobacteria switched between photolithoautotrophic and
photoorganoheterotrophic metabolism prior to the evolution of cyanobacteria
with simultaneous, constitutive expression of genes allowing both types of
metabolism. It is also likely that phototrophy based on purple retinal
pigments similar to the chromoprotein bacteriorhodopsin, discovered in
halophilic Archaea, may have dominated prior to the development of
photosynthesis (DasSarma and Schweiterman, 2018). The activity of these
early microorganisms and subsequent accumulation of oxygen in the atmosphere
paved the way for the evolution of plants, and there is a large and diverse
body of evidence that the plastids of algae and higher plants evolved from
free-living bacteria by endosymbiosis involving endosymbiotic gene transfer
(Zimorski et al., 2014) as well as horizontal gene transfer (Archibald,
2015) (Fig. 3b).
Evolution of higher plants and development of vegetation has had a
substantial effect on mineral weathering. The first well-differentiated
forests appeared in the Devonian, and increases in the volume of roots from
the Silurian to the Devonian are associated with increases in clay
enrichment and chemical weathering in subsurface horizons and drawdown of
atmospheric CO2 (Retallack, 1997). Dissolution of bedrock, accelerated
by growth of plants and enhanced weathering of silicates, resulting in
HCO3- carried to the sea and precipitated as carbonates, would
have led to removal of CO2 from the atmosphere. Further, the large drop in
CO2 during the Devonian 400–360 Myr ago is thought to be associated with
the rise of land plants and spread and development of forests (Berner,
1997).
The ubiquitous distribution of microorganisms today suggests that plants are
not stand-alone entities but should be considered from a holistic
perspective, as holobionts, including the full diversity
of the many different microorganisms associated with them
(Vandenkoornhuyse et al., 2015). Almost all plant roots are colonised by
microbial symbionts, making it difficult to quantify the separate
contributions of plants and associated microorganisms to mineral weathering.
There is broad agreement that fungi are important biotic agents of
geochemical change (see Gadd, 2010, 2013a, b, 2017) and that coevolution of
fungi and plants has enabled them to have increasing influence as
biogeochemical engineers (Fig. 3c–g). Fungi exert significant influence on
biogeochemical processes, especially in soil, rock and mineral surfaces and
the plant root–soil interface where mycorrhizal fungi are responsible for
major mineral transformations, redistribution of inorganic nutrients and
flow of C. They are important components in rock-inhabiting communities with
roles in mineral dissolution and secondary mineral formation. The ubiquity
and significance of lichens as pioneer organisms in the early stages of
mineral soil formation, and as a model for understanding weathering in a
wider context, have been discussed by Banfield et al. (1999) and Chizhikova
et al. (2016). In lichens, photosynthetically fixed C is transferred from
the photobionts (green algae and cyanobacteria) to a fungal thallus in
contact with the mineral surfaces. Non-photosynthetic prokaryote assemblages
are also present in a zone of microbially mediated weathering where mineral
surfaces are covered in complex mixtures of high-molecular-weight polymers,
clays and oxyhydroxides, and mineral weathering is accelerated via
polymer-mediated dissolution, transport or recrystallisation. Increasing
evidence suggests that these bacteria are integral components of lichen
thalli, contributing to the overall fitness of the lichen in functionally
diverse ways (Grube et al., 2015) and that the structure of the bacterial
microbiome is influenced by the identity of the photoautotrophic symbionts
(Hodkinson et al., 2012). Whilst the functional roles of these bacteria are
still poorly understood, some have been demonstrated to solubilise phosphate
(Sigurbjörnsdóttir et al., 2015). There are similarities in the
carbon compounds produced by fungi forming lichens and other fungi, but in
later successional stages other types of symbiosis occur, involving
mycorrhizal plants. Furthermore, throughout evolution successive increases in the
size of plants (Quirk et al., 2015) have allowed larger amounts of carbon to
be allocated to larger root systems and greater amounts of mycorrhizal
mycelium and exudates – increasing their potential for interacting with
mineral substrates. Although the genetic potential for hydrolytic
decomposition of cellulose and other plant cell wall components has
contracted in comparison with their saprotrophic ancestors (Kohler et al.,
2015; Martin et al., 2016), saprotrophic fungi also exude the same types of
carbon compounds as ectomycorrhizal fungi, including organic acids.
Paxillus involutus, an ectomycorrhizal species derived from a clade of brown-rot fungi, appears
to have retained the non-enzymatic Fenton chemistry used by brown-rot fungi
to extract N from organic matter (Nicolás et al., 2019). P. involutus produces
oxalate and weathers minerals, and it is possible that different organic
acids have multiple effects beyond weathering. However, as far as we are aware,
differences in organic acid production have not yet been studied
comprehensively from an evolutionary perspective. Fahad et al. (2016)
compared mobilisation of base cations and P from granite particles by
saprotrophic and ectomycorrhizal fungi in vitro and found statistically higher
levels of accumulation of Mg, K and P by the ectomycorrhizal fungi, but only
a few species were examined and further systematic comparisons of larger
numbers of species need to be conducted to establish the generality of this
result. Symbiotic ectomycorrhizal fungi are thought to have evolved
repeatedly and independently from saprotrophic precursors, so there should
have been selection for ectomycorrhizal fungi that can efficiently mobilise
nutrients and transfer them to the large sinks created by their host trees.
However there have also been multiple reversals from the symbiotic habit to
the free-living saprotrophic habit (Hibbett et al., 2000), so caution should
be exercised in generalisations based on lab experiments. In vitro experiments, in
which fungi are cultured without their host plants, also introduce artefacts
since the host plants act as important sinks for weathering products,
preventing feedback inhibition of weathering processes due to accumulation
of reaction products.
The effects of evolutionary advancement in plants and mycorrhizal associations in the geochemical carbon cycle, increasing the
weathering of calcium (Ca)-, phosphorus (P)-, and silicon (Si)-bearing minerals and generating clays. Plants and their mycorrhizal
fungi have increased the rates of dissolution of continental silicates, especially calcium silicate (CaSiO3), and apatite
(Ca phosphate-CaPO4), but a portion of the Ca, P and Si released from rocks is washed into the oceans where these elements
increase productivity. Some of the Ca and P ends up in limestone and chalk deposits produced by marine organisms such as
corals and foraminifera, thereby sequestering carbon dioxide (CO2) that was dissolved in the oceans into calcium carbonate
(CaCO3) rock for millions of years. Dissolved Si is used in sponges, radiolarians and diatoms that can accumulate on the sea
floor. The ocean sediments are recycled by subduction or uplift by tectonic forces, with volcanic degassing and eruptions of
base-rich igneous rocks such as basalt returning Ca, P, Si and other elements back to the continents, thereby reinvigorating
ecosystems with new nutrient supplies through weathering. Note for simplicity that magnesium is not shown in the figure but
follows parallel pathways to Ca and is co-involved in sequestering CO2 into dolomitic limestones. aq, liquid state; g, gaseous
state. (Figure is reproduced with permission: Leake and Read, 2017.)
Many studies of ectomycorrhizal influence on weathering rates have been
performed over short periods and do not always provide clear evidence that
processes observed at the laboratory scale play a significant role in
“soil-scale” mineral dissolution rates. Smits et al. (2014) used a
vegetation gradient from bare soil, via sparse grass to Norway spruce forest
in a natural lead-contaminated area in Norway to study long-term effects of
vegetation on apatite weathering in moraine deposited at the end of the last
glaciation. Vegetation had a strong stimulatory effect on apatite weathering,
and 75 % of the variation in apatite weathering could be explained by soil
pH, but the effect of plant roots and mycorrhizal symbionts on this process
could not be separated. In the top 20 cm of the mineral soil, an additional
mechanism, not mediated by pH, enhanced dissolution of apatite. The authors
suggested this might be caused by organic acids, leading to higher
concentrations of the organic–metal complexes on the mineral surfaces but
that the origin of these acids was probably not ectomycorrhizal fungi since
these fungi were absent in the grass vegetation at the highest pH area of
the vegetation gradient. Under these conditions, the biomechanical and
chemical effects of ectomycorrhizal fungi on apatite weathering seemed to be
minor, but these effects are probably dependent on the nutrient status of
the forest. Enhanced colonisation of apatite by ectomycorrhizal hyphae in
laboratory systems (Rosling et al., 2004; Smits et al., 2012) is also
commonly found under field conditions, but only when P availability is low
(Rosenstock et al., 2016; Bahr et al., 2015; Almeida et al., 2019). The
potential for weathering by ectomycorrhizal fungi is probably much higher
under these conditions and the nutrient status of the forest should be
considered when biological weathering rates are quantified, at least for
apatite weathering, where P status has a strong effect on fungal
colonisation of apatite. In contrast, no enhanced colonisation of biotite
and hornblende by ectomycorrhizal hyphae was found in Norway spruce forests
in the Czech Republic under low K or Mg availability (Rosenstock et al.,
2016). This suggests that ectomycorrhizal fungi have a smaller potential to
enhance weathering of these minerals compared to apatite. However, these
results should be treated with caution since no quantitative or chemical
estimates of the mineral weathering were made, and use of ergosterol-based
estimates of fungal biomass as a proxy for weathering can be
misrepresentative, since some ectomycorrhizal fungi that actively release
LMW organic acids may not invest much carbon in their own biomass. Further
investigations using RNA-based analysis of active microbial communities,
combined with temporal assessment of weathering kinetics, should reveal the
true potential of microorganisms in biogeochemical weathering in forest
ecosystems. Effects of N-fixing microorganisms on weathering activity have
not been studied in detail but the resulting inputs of N might be expected
to drive growth and increase demand for rock-derived nutrients. Recent
studies by Perakis and Pett-Ridge (2019) based on uptake of strontium (Sr)
isotopes suggest that nitrogen-fixing red alder (Alnus rubra) trees can take up
significantly more rock-derived Sr than five other co-occurring tree
species, although the mycorrhizal fungi colonising these trees were not
identified.
Fungal weathering of rocks and minerals through biomechanical and
biochemical attack has been studied extensively. Proton-promoted dissolution
is supplemented by ligand-promoted dissolution of minerals by strong
chelators such as oxalic and citric acid that may act synergistically with
siderophores. Secondary minerals may be deposited as carbonates, oxalates, or
other mycogenic minerals and mineraloids, and the role of “rock-building
fungi” has been discussed in addition to the role of “rock-eating fungi”
(Fomina et al., 2010). Fungi are prolific producers of oxalate, and
oxalotrophic bacteria are capable of oxidising calcium oxalate to calcium
carbonate. Since the oxalate is organic in origin, and half its C is
transformed into mineral C with a much longer residence time, this process
represents a potential major sink for sequestration of atmospheric C
(Verrecchia et al., 2006). Precipitation of carbonate minerals by
microorganisms during silicate weathering has also been discussed by Ferris
et al. (1994) in relation to its potential role as a sink for atmospheric
CO2. The oxalate–carbonate pathway may not be important in boreal
forest soils; however the African oxalogenic iroko tree Milicia excelsa, together with
associated saprotrophic fungi and bacteria, enhances carbonate precipitation
in tropical Oxisols, where such accumulations are not expected due to the
acidic nature of the soil (Cailleau et al., 2011), and the same phenomenon
has been demonstrated in acidic soils of a Bolivian tropical forest
(Cailleau et al., 2014). Studies of bacterial assemblages in soil associated
with ectomycorrhizal roots of Pinus massoniana and Quercus serrata have revealed enrichment of oxalotrophic
bacteria using the oxalate–carbonate pathway, representing a potential
long-term sink for photosynthetically fixed carbon derived from the
atmosphere (Sun et al., 2019a). The role of microorganisms in dissolution
and modification of karst stones such as limestone and dolomite has also
been studied (Lian et al., 2010, 2011). Microbially mediated chemical
corrosion and precipitation in surface and underground water can play a role
in pedogenesis and provide a sink for atmospheric CO2, and the role of
carbonic anhydrase in hydrating atmospheric CO2 to HCO3- has
been investigated in relation to changes in CO2 concentration and
availability of Ca2+ (Xiao et al., 2014, 2015). The results of the
latter study suggest that the importance of microbial carbonic anhydrase on
silicate weathering and carbonate formation may be higher at current
CO2 levels than under primordial conditions 2 Myr ago when CO2
levels were much higher.
Rapid decreases in soil respiration following the girdling of forest trees
(Högberg et al., 2001) suggest that the flux of current assimilates to
mycorrhizal roots is directly connected to the supply and respiration of C
in soil. In another study (Högberg and Högberg, 2002), extractable
DOC in a 50-year-old boreal forest was 45 % lower in girdled plots than
in control plots, suggesting a large contribution by roots and associated
fungi to soluble-C pools, although the contribution of these two components
could not be determined separately. Biogeochemical weathering of silicate
rocks is a key process in the carbon cycle (Pagini et al., 2009), and, although
consumption of CO2 by weathering is small compared with transfers
associated with photosynthesis and respiration, it is the dominant sink in
global carbon balance and controls atmospheric CO2 and climate patterns
at scales of millennia or longer (Goudie and Viles, 2012).
The geoengineering potential of artificially enhanced silicate weathering is
now increasingly well established (Köhler et al., 2010),
and addition of pulverised silicate rocks to different croplands has been
advocated as an effective strategy for global CO2 removal (CDR) and
ameliorating ocean acidification by 2100 (Taylor et al., 2016; Beerling et
al., 2018). Large-scale field trials are now in progress (http://lc3m.org/, last access: 20 March 2020), but basic information about the way in which different
microorganisms drive the sequestration processes in different soil types is
still missing. Recent studies on carbonate weathering by ectomycorrhizal
fungi colonising tree roots (Thorley et al., 2015) suggest that
ectomycorrhizal tree species weather calcite-containing rock grains more
rapidly than arbuscular mycorrhizal (AM) trees because of greater
acidification by the ectomycorrhizal trees. Weathering and corresponding
alkalinity export to oceans may increase with rising atmospheric CO2 (Andrews and Schlesinger, 2001) and associated climate change,
slowing rates of ocean acidification.
Transfer of increasing amounts of photosynthetically derived carbon to
ectomycorrhizal fungi and improved colonisation of mineral substrates during
evolution of plants (Quirk et al., 2012, 2014a) are consistent with the idea
that weathering of silicate minerals and sequestration of C into ocean
carbonates has led to drawdown of global CO2 levels during the rise of
ectomycorrhizal trees over the past 120 Myr (Taylor et al., 2011; Morris et
al., 2015). However, the relative constancy of atmospheric CO2 levels
and absence of even further reductions over the final 24 Myr of the Cenozoic
have been attributed to a negative feedback mechanism caused by CO2
starvation (Beerling et al., 2012) that is predicted, by numerical
simulations, to reduce the capacity of the terrestrial biosphere to weather
silicate rocks by a factor of 4. Differences in the magnitude of carbon
transfer from plants to different types of mycorrhizal fungal symbionts and
the physiological mechanisms regulating this transfer are influenced by the
biotic and abiotic environment, as well as the life history and evolutionary
origins of the symbiosis. Common-garden experiments (Koele et al.,2012),
using sister clades of plants (with different types of mycorrhiza), might
provide a suitable way of comparing functional groups, but broad
generalisations should be made with extreme care since there is a high
degree of context dependency (Field et al., 2017). Ericoid mycorrhizal fungi
can produce copious amounts of LMW organic acids that solubilise inorganic
zinc compounds (Martino et al., 2003), but there are so far no systematic
studies of their role in different weathering interactions in comparison to
other fungi. Further comparative studies of the role of different types of
mycorrhizal symbioses in mineral weathering may shed light on the different
physiological mechanisms involved. Soil microorganisms can have strong
effects on plant resource partitioning and it has been shown (Ryan et al.,
2012) that Kennedia species inoculated with arbuscular mycorrhizal fungi allocated
lower amounts of carboxylates to the rhizosphere but had higher
concentrations of P than non-inoculated plants, presumably using less
strongly sorbed forms of P.
Inferences about evolutionary development of weathering have been drawn
using vertical scanning interferometry to study “trenching” of silicate
mineral surfaces (basalt) buried under different tree species growing in an
arboretum (Quirk et al., 2012) and suggest that trenching and hyphal
colonisation increase with evolutionary progression from AM fungi to
ectomycorrhizal fungi, and with progression from gymnosperm to angiosperm
host plants. It is suggested that this evolutionary progression resulted in
release of calcium from basalt by ectomycorrhizal gymnosperms and
angiosperms at twice the rate achieved by AM gymnosperms and that forested
ecosystems have become major engines of continental silicate weathering,
regulating global CO2 concentrations by driving calcium export into
ocean carbonates (Quirk et al., 2012) (Fig. 4). Additional
laboratory studies of the same tree species using different CO2
environments suggest that weathering intensified during evolutionary
progression from AM fungal symbionts to ectomycorrhizal symbionts and that
calcium dissolution rates were related to photosynthate energy fluxes and
higher during a simulated past CO2 atmosphere (1500 ppm) under which
ectomycorrhizal fungi evolved (Quirk et al., 2014b).
Summary
Microorganisms have interacted with minerals for billions of years,
enriching the atmosphere with oxygen and shaping the evolution of minerals
long before the evolution of land plants. There is strong evidence that the
plastids of algae and higher plants evolved from free-living bacteria
through endosymbiosis, and plants have continued to evolve in conjunction
with microorganisms through symbiotic alliances (mycorrhiza, actinorhiza,
rhizobia, plant-growth-promoting rhizobacteria (PGPR), etc.) such that they
are really holobionts – assemblages of organisms. This enabled the
holobionts to become successively more efficient biogeochemical engineers.
Hypotheses have been advanced concerning the evolutionary development of
weathering and differing contributions of different types of mycorrhizal
symbiosis. Further advances in understanding will require more studies of
different combinations of plant and fungal species, accompanied by rigorous,
DNA-based, in situ identification of the different fungal symbionts. However, the
magnitude of carbon transfer to different types of mycorrhizal fungal
symbionts and the physiological mechanisms regulating this transfer are
highly context dependent, and advances in knowledge will require sound
ecological understanding, based on integration of a diverse array of biotic
and abiotic factors. Better information is still required on the identity of
bacteria and fungi colonising bedrock outcrops and other mineral substrates
in forests. The diversity of these communities is high and it is important
to identify the particular taxa that are most active in competing for plant-derived C and to identify the amounts and chemical forms in which it is
delivered to mineral surfaces. Use of 13C-based stable isotope probing
is likely to be helpful in identifying the most active taxa delivering
plant-derived C to mineral surfaces. Analysis of the chemical composition of
compounds involved will necessitate further studies using nanoSIMS, NMR and
Fourier transform infrared (FTIR) spectroscopy. Improved understanding of weathering at an ecological
level requires better knowledge about the processes involved in
sequestration of atmospheric CO2, and further investigation of the forms
in which C is sequestered during weathering in forests is necessary.
Weathering processes are impacted by different environmental conditions and
types of forest management and further studies are required to investigate
how these are impacted by changes in atmospheric CO2 concentration and
effects of N deposition and fertilisation.
Methods using stable isotopes
Stable isotopes, especially of Ca and Sr, have been used extensively to
source the origin of Ca in drainage water; when applied to plant tissues,
they can be used to trace plant nutrients back to their primary source.
Isotope tracing has been mostly used to study apatite weathering. P has no
stable isotopes, and the mobilisation and uptake dynamics of apatite can
therefore only be studied via the Ca ion (or potentially the
18O/16O in the phosphate group). In most rocks and soils, apatite
is the sole primary P source. However, its contribution to the soil solution
Ca pool is minor compared with other minerals. If the Ca isotope ratio in
the plant is more similar to the signature in apatite than to the signature
in the soil solution, then it indicates that the plant directly acquires Ca
from apatite. Blum et al. (2002) applied this technique to a temperate mixed
forest using Ca:Sr ratios in soil water, minerals in the soil, and different
mycorrhizal and non-mycorrhizal trees. The authors concluded that direct
calcium uptake by ectomycorrhizal fungi weathering apatite in the parental
material could compensate for calcium loss in base-poor ecosystems. Data on
element ratios should, however, be interpreted with care because of high
variation in Ca:Sr ratios in different plant tissues and limited
understanding of the cycling of these elements in plants (Watmough and
Dillon, 2003), as well as contradictory data of Dijkstra and Smits (2002)
(see below) that suggest the conclusion of Blum et al. (2002) is overstated.
Field studies using mesh bags containing microcline and biotite, buried in
Swedish Picea abies forests (Wallander et al., 2006), used the 87Sr:86Sr ratio
to calculate the fraction of Sr in the mycorrhizal root tips that had
originated from the minerals. Although the total amounts of Sr released from
the minerals could not be calculated since the total plant biomass enriched
with 87Sr was unknown, the study clearly demonstrates the potential of
ectomycorrhizal fungi to mobilise and take up nutrients such as Ca and K
from microcline and biotite under field conditions.
In many forest ecosystems, plant-available pools of Mg, Ca and K are
assumed to be stored in the soil as exchangeable cations adsorbed on the
cation exchange complex (exchangeable pools). However, other storage forms
of Mg, Ca and K that have not been fully characterised may play an
important role in plant nutrition and biogeochemical cycles and be
plant-available on very short timescales (< 1 d). Isotopic
dilution techniques using the stable isotopes 26Mg, 44Ca and
41K have been developed (van der Heijden et al., 2018) to trace and
quantify the pools of Mg, Ca and K (isotopically exchangeable pools) that contribute directly to equilibrium processes
between the soil water and the soil in a hardwood forest. These show that isotopically
exchangeable pools of Mg, Ca and K are greater than traditionally measured
exchangeable pools. Storage forms of Mg, Ca and K in the isotopically
exchangeable pool could include chelation with soil organic matter,
retention on soil aluminium and iron oxides and hydroxides through phosphate,
and/or organic acid bridges and site-specific adsorption. The isotopic
dilution method is a relevant tool to quantify the plant-available pools of
Mg, Ca and K on short timescales (source and sink pools) and is a very
promising approach to characterise and quantify the processes responsible
for the depletion and/or replenishment of these pools over longer timescales.
Field studies of small rock fragments isolated from a Finnish P. sylvestris forest with
Tricholoma matsutake fruiting bodies (Vaario et al., 2015) revealed the presence of T. matsutake on 97 %
of the rock fragments, and laboratory assays using X-ray diffraction
confirmed the ability of the fungus to absorb some trace elements directly
from the rock fragments, but uptake of Mg and K did not appear to be
significant. In contrast, laboratory studies of the capacity of different
fungi to mobilise P and base cations from granite particles (conducted
within QWARTS) (Fahad et al., 2016) suggest that some ectomycorrhizal fungi
can mobilise and accumulate significantly higher concentrations of Mg, K and
P than non-mycorrhizal fungi. The mycorrhizal fungi can fractionate Mg
isotopes, discriminating against heavier isotopes, and we found a highly
significant inverse relationship between δ26Mg tissue
signatures and mycelial concentration of Mg (Fig. 5). This provides a
theoretical framework for testing hypotheses about fungal weathering of
minerals in future experiments. If active mobilisation and uptake of lighter
24Mg isotopes results in relative enrichment of heavy Mg isotopes left
in soil solution and soil, this should be evident in areas of active
weathering. Mesocosm experiments, conducted within the QWARTS project, employing a gradient of increasing organic
matter depletion to simulate progressively more intense forest biomass
harvesting, revealed significant and successive enrichment of 26Mg
signatures in the soil solution in the B horizon, associated with increased
availability of organic matter and resultant increases in plant and fungal
biomass (Fig. 6). No such enrichment was found in other horizons or in
systems without plants (and therefore without mycorrhizal fungi). This
suggests that significant biological weathering of Mg takes place in the B
horizon, driven by higher plant biomass that enables improved carbon
allocation to the fungal mycelium and also constitutes a larger sink for
uptake of mobilised base cations. Although the experiments provide strong
support for the idea of biologically driven mobilisation of Mg from B-horizon mineral soil, the process was not sufficient to maintain optimal
tree growth in systems with a severely reduced organic matter pool. In
addition, studies carried out under both field and laboratory conditions
show that Mg isotope fractionations are controlled by the same biological
factors in the critical zone, defined as the outer layer of earth from
vegetation to the soil. Silicate rocks show a relatively small range of
variation in Mg isotopic ratios (denoted as δ26Mg) (Bolou-Bi et
al., 2009; Shen et al., 2009; Uhlig, et al., 2017). During the weathering of
these rocks at the watershed level, it was revealed that isotopic fractionation
of Mg isotopes was in favour of light isotopes in soil solution, while the
soils were enriched in heavy isotopes (Pogge von Strandmann et al., 2008;
Tipper et al., 2010). Studies conducted in forest ecosystems (Bolou-Bi et
al., 2012; Mavromatis et al., 2014; Uhlig et al., 2017) indicate variation
in soil solution signatures of surface soil layers, suggesting a role of
vegetation through the Mg isotope cycle (uptake and litterfall), soil
exchangeable fraction and rainwater, and light Mg isotope return
via litterfall. In deeper soil horizons, however, the soil solution
signatures may be the result of two additional processes: (a) the mineral
dissolution leaching the light isotope into solution and subsequently
weathered minerals being systematically enriched in heavy Mg isotopes relative
to fresh rock, and (b) clay formation and/or Mg adsorption removing the
heavy Mg isotope from soil solution (Huang et al., 2012; Opfergelt et al.,
2014). Mg isotope fractionation has also been observed under laboratory
conditions during the dissolution of primary minerals (Wimpenny et al.,
2010).
Bivariate plots of δ26Mg (‰) versus Mg concentration (mg g-1) in mycelia of ectomycorrhizal and nonmycorrhizal fungi
grown on mineral-free modified Melin-Norkrans (MMN) medium amended with granite particles. The fungi were grown on
cellophane membranes covering the growth substrates in Petri dish microcosms. Open blue symbols represent nonmycorrhizal
fungi and closed brown symbols represent ectomycorrhizal fungi. (Figure is reproduced with permission; Fahad et al., 2016.)
In studies of Ca isotope cycling in a forest ecosystem, it appears that the
soil solution and exchangeable fraction generally display enrichment in the
heavy isotope compared to soil particles, bedrock and rainwater (Holmden and
Bélanger, 2010; Hindshaw et al., 2011). However, the soil solution
isotope signatures are not the simple result of weathering processes in
soils because the congruent dissolution of rock or mineral observed in lab
and field conditions did not cause any measurable Ca isotope fractionation
(Hindshaw et al., 2011; Ryu et al., 2011; Cobert et al., 2011). This
suggests that another process, such as the preferential uptake of the light
Ca isotope (40Ca) by vegetation, decreases the soil solution Ca isotope
ratio in the upper horizon in addition to light Ca isotope return via
litterfall (Page et al., 2008; Holmden and Bélanger, 2010). In deeper
soil horizons, soil solution δ44/40Ca may result from the
dissolution of minerals such as apatite. Interestingly, experiments by
Dijkstra and Smits (2002) indicate that most of the Ca taken up by trees
comes from litter recycling. In a comparable mixed forest, also in the
north-eastern United States, the annual Ca import from weathering in the
rooting zone is less than 0.3 % of the annual Ca uptake, which was a
flux 4-fold smaller than the annual atmospheric deposition (Dijkstra and
Smits, 2002). Inputs of nutrients such as P, from atmospheric deposition, may
also be significant in coastal Fynbos systems (Brown et al., 1984) and the
Florida everglades (Redfield et al., 2002). However, the data from our
QWARTS experiments suggest that mobilisation of Mg may function differently
in boreal coniferous forests, with higher amounts being mobilised from
inorganic substrates in the B horizon.
Mycorrhizal fungi play a central role in mobilising N and P from organic
substrates, and when these are depleted N and P limit tree growth, resulting
in reduced C supply to the mycorrhizal mycelium and reduced capacity for
mobilisation of base cations from the mineral horizons. Although
mobilisation of Mg from the B horizon was sufficient to support increased
biomass production in systems supplied with extra organic material (Fig. 6),
it was not sufficient to compensate for losses of base cations when organic
material was most depleted. The results of these experiments are therefore
consistent with the predictions of modelling that, under intensive forestry
with removal of organic residues, base cation supply will not be sustainable
in the long term. Intensive, sustained harvesting of biomass may lead to N
limitation before base cations become limiting. Applications of different
fertilisers (Xiao et al., 2017) or inadvertent N deposition (Averill et al.,
2018) may have negative effects on both weathering and C sequestration.
Smits and Wallander (2017) advocate detailed studies of the liquid chemistry
of local weathering sites at the micrometre scale, together with upscaling
to soil-scale dissolution rates. The authors suggest that future
research should focus on whole ecosystem dynamics, including the behaviour
of soil organic matter, and that early-stage primary succession ecosystems
on low reactive surfaces, such as fresh granites, should be included. Smits
and Wallander (2017) also recommend the use of stable isotopes by choosing
minerals and soils with distinct isotope ratios.
Summary
Experiments using stable isotopes have the potential to improve understanding of
the roles played by different groups of microorganisms in biological
weathering. In vitro studies of base cation mobilisation from granite particles so
far suggest that symbiotic mycorrhizal fungi may be more efficient at
mobilising Mg, K and P than saprotrophic fungi, but it is necessary to test a
wider range of species before such broad conclusions can be drawn. Care
should also be exercised in interpreting experiments conducted in vitro in the
absence of host plants, since these provide important sinks for mobilised
nutrients that could otherwise retard weathering reactions should they
accumulate. Fractionation of stable Mg isotopes by mycorrhizal fungi, with
preferential uptake of lighter isotopes, results in enriched levels of
26Mg in soil solution, and laboratory experiments with reconstructed
podzol profiles have demonstrated that this enrichment occurs primarily in
the B horizon. The data suggest that this pathway may be of significance in
the field but reductions in (N-containing) organic matter resulted in
reduced tree growth and reduced Mg uptake, suggesting that increased
biological weathering of Mg is unlikely to compensate for losses of Mg
through organic matter removal if N is also limiting. However, K and P were
also deficient in this experiment so conclusions should be drawn with care.
Similar experiments with isotopes of other elements may reveal wider
information about patterns of nutrient uptake. In addition to their possible
weathering effects, mycorrhizal fungi play important roles in N acquisition
from organic substrates, illustrating how decomposition and weathering are
intercoupled.
Mesocosms containing reconstructed podzol soil profiles with different amounts of organic (O) horizon material to
simulate different intensities of forest harvesting. (a) No O horizon; (b) 50 % thickness O horizon; (c) normal (100 %) thickness
O horizon; (d) 150 % thickness O horizon. The histograms show levels of enrichment of 26Mg in soil solution extracted
from the O (organic), E (eluvial) and B (illuvial) horizons. The upper part of each diagram represents systems incubated
without plants, the lower part of each diagram represents systems containing Pinus sylvestris seedlings (as illustrated). Note
that the seedling growth is proportional to the amount of organic soil, from which ectomycorrhizal fungi mobilise N. The
enrichment of 26Mg in the soil solution becomes greater and greater with increasing plant growth (and therefore increasing
Mg uptake) – but only in the B horizon, because there is discrimination against uptake of the heavy isotope. This suggests that
the B horizon is the primary site of active mineral weathering and Mg uptake. Extensive colonisation of roots and organic and
mineral substrates by ectomycorrhizal mycelia is visible. Horizontal scale bar in (a) is equal to 5 cm.
Modelling of biological weathering in forest soilsDevelopments and improvements in modelling biological
weathering
Models greatly improve our ability to quantify weathering rates and how they
change over time. Akselsson et al. (2019) present an extensive review of
methods for estimating weathering rates in forest soils. These range from
mass-balance budget calculations (e.g. Simonsson et al., 2015) and
gravimetric approaches (Turpault et al., 2009) to the depletion method
based on the elemental concentration differences between weatherable and
unweatherable minerals (such as zirconium bound in zircon or titanium in
rutile) (Stendhal et al., 2013) to dynamic models based on the transition
state theory (Erlandsson et al., 2016). These methods address, in different
ways, the role of biological processes in weathering (Rosling et al., 2009).
Here we attempt to describe the major approaches to implementing important
biological processes into weathering rate estimates over the last decade.
Catchment and ecosystem mass-balance approaches have been widely employed to
estimate mineral weathering rates (Price et al., 2013, Hartmann and
Moosdorf, 2011). Application of machine learning approaches (Povak et al.,
2014) can further increase the utility of mass-balance approaches for
evaluating the potential importance of different processes to weathering
rates. Biomass accumulation emerges, in many simulations (Wilcke et al.,
2017; Zetterberg et al., 2016), as a key variable in mass-balance estimates
of mineral weathering and a major source of uncertainty (Simonsson et al.,
2015; Zetterberg et al., 2016). Furthermore, the derivative nature of the
mass-balance approach reduces its value for assessing the mechanisms that
control weathering rates, reducing their suitability to predict future
weathering rates under changing conditions.
Taylor et al. (2011) built on a geochemical model developed by Banwart et al. (2009), which attempts to quantify the contribution of biologically
derived protons and ligands to mineral weathering rates and distinguishes
between vegetation that forms arbuscular (AM) mycorrhizal associations and
vegetation that forms ectomycorrhizal (EM) associations. Their model
assumes that AM fungi do not exude significant amounts of organic acids
while EM fungi do, and it models the activity of that exudation as that of
oxalic acid. They also divide the soil volume into an area of immediate
proximity to mycorrhizal hyphae, the mycorrhizosphere and the bulk soil.
When they applied their model over the last 200 Myr they observed that the
drawdown of global atmospheric CO2 levels over the last 120 Myr could
largely be attributed to the emergence and diversification of angiosperms
and the spread of EM fungi. However, in addition to organic acid exudation,
hyphal length density, which defined the volume of the mycorrhizosphere, was
parameterised to be 25-fold greater in EM-dominated ecosystems than AM-dominated systems. Modelled soil chemistry and the resulting terrestrial
carbon sink were also highly sensitive to hyphal length density. Taylor et al. (2012) further developed this weathering model based on mycorrhizal
association type and coupled it to a dynamic global vegetation model and
validated it against a global dataset of watershed flux data. The resulting
model, when applied over the last 200 Myr, indicated that biological
weathering was stronger in the distant past than today and estimated that
vegetation and mycorrhizal fungi have increased terrestrial weathering rates
by a factor of 2. While their model performed reasonably well in the
validation across a global series of catchment data, their findings did not
support a distinct dichotomy in weathering behaviour between AM-dominated
and EM-dominated ecosystems. Quirk et al. (2014a) build on the model
developments of Taylor et al. (2011, 2012) to illustrate the potential for a
feedback between atmospheric CO2 levels and biological weathering
rates, such that, as CO2 levels increase, global plant productivity and
autotrophic soil inputs of protons and organic acids do so as well,
stimulating biological weathering and serving as a negative feedback to
increasing CO2 levels. As CO2 levels decrease, so does biological
weathering. This sequence of models develops hypotheses concerning the role
of land plants in the geology of earth and the global biogeochemical carbon
cycle, with a framework to account for differential biological weathering
activity by distinct vegetation types. While considerable evidence exists
pointing to the potential for ectomycorrhizal fungi to be more potent
weathering agents than AM fungi, field studies comparing weathering rates in
paired AM- and EM-dominated forests have failed to find significant
differences in mineral weathering rates (Koele et al., 2014; Remiszewski et
al., 2016). Future applications utilising rhizosphere or mycorrhizosphere vs.
bulk soil volumes should place more emphasis on the choice of hyphal length
densities and should likely use functions, as opposed to fixed parameters,
that depend on plant type as well as plant productivity and nutrient status
to describe fine-root and mycorrhizal hyphal root lengths.
Roelandt et al. (2010) coupled a reactive transport model to the
Lund-Potsdam-Jena global dynamic vegetation model, which they termed
Biosphere-Weathering at the Catchment Scale (B-WITCH), and were able to
model base cation efflux accurately from the Orinoco watershed. They
concluded that vegetation exerts a major role on mineral weathering rates
but that this role is primarily hydrological, via evapotranspiration fluxes.
However, while their model did feature organic ligand-promoted dissolution,
the source of those ligands was decomposition only, and they treat the entire
rooting zone as a single interconnected solution. Furthermore, they do feature
plant functional types, those functional types do not correspond to
below-ground physiology or mycorrhizal association. The B-WITCH model appears
to reflect the most mechanistic approach amongst global dynamic vegetation
models to estimating mineral weathering rates, but additional processes may
need to be implemented to capture the influence of biology on mineral
weathering rates.
Maher et al. (2010) applied the reactive transport geochemical model
CrunchFlow, which estimates weathering rates based on experimentally derived
dissolution equations for individual minerals, to examine the effect of
fluid residence time, which in turn controls the transport of weathering
products away from mineral surfaces, on mineral weathering rates. They
observed a strong inverse relationship between fluid residence time and
weathering rates and interpreted this as clear evidence for transport
control of weathering rates in natural ecosystems. Lawrence et al. (2014)
coupled an organic acid module to the CrunchFlow model to examine the
potential role of organic acids, modelled as oxalic acid, on mineral
weathering rates. They observed that the primary effect of oxalic acid was to
increase soluble Al but decrease free Al3+ concentrations in solution;
mineral weathering was enhanced near the zone of oxalic acid production (the
topsoil) but decreased further down the profile. The description of organic
acid levels as the product of production and decomposition processes and the
geochemical description of ligand-promoted chelation, dissolution and
transport may be useful to model the effects of
biological exudates on mineral weathering rates and adaptable across a range
of models. Winnick and Maher (2018) developed CrunchFlow to examine the
dependence of mineral weathering rates on gaseous and dissolved CO2
concentrations and observed a very strong relationship between weathering
rates and soil CO2. They further suggested that this may be an important
mechanism by which soil respiration of vegetation (and mycorrhizal fungi)
may stimulate mineral weathering.
Mineral weathering is dynamically simulated in the PROFILE and ForSAFE
models, which have been widely used for unsaturated soils (for recent
examples see Akselsson et al., 2016; Erlandsson et al., 2016; Belyazid et
al., 2019; Phelan et al., 2014). In ForSAFE, tree cover, soil microbes and
related biological processes are also integrally simulated. Trees are
assumed to affect weathering through a number of causal pathways. Firstly,
trees have a direct negative influence on soil moisture through
transpiration. The consequent reduction in soil moisture limits weathering,
as the latter is directly dependent on wetted mineral surface area. Water
uptake also leads to an increase in element concentrations, drawing the soil
solution closer to saturation and acting as a retarding brake on weathering
(Erlandsson et al., 2016). Secondly, nutrient uptake reduces the
concentration of base cation weathering products, releasing these brakes and
thereby promoting weathering rates. Thirdly, plants are responsible for the
production of organic matter, which, through below-ground allocation and
litter fall, feeds soil organic carbon, dissolved organic carbon and
CO2 concentrations. Both organic radicals and higher soil CO2
pressure have positive influences on weathering rates. At the same time, the
mineralisation of litter also releases the base cations, thus increasing
element concentrations and thereby slowing down weathering rates. Fourthly,
plants have a direct effect on soil solution proton concentration, which
promotes higher mineral weathering. Plants can lower pH through the
production of organic matter, but most importantly through the uptake of
positively charged cations and release of protons to counterbalance charge.
Lower pH promotes higher weathering rates but also the solubility of
aluminium ions whose higher concentrations act as weathering brakes. The net
effect on weathering, i.e. the balance between the positive effect from
lower pH and the negative from higher aluminium concentrations, may differ
depending on soil properties. The contribution of biological weathering may
be improved by division of the soil volume into rhizosphere or
mycorrhizosphere and bulk soil portions. Process descriptions of root and
hyphal influence on the solution and surface chemistry within the
rhizosphere and/or mycorrhizosphere could also be improved. Division of DOC into
discrete chemical functional classes (promoting vs. inhibitory, actively
exuded vs. incomplete decomposition products) could increase our
understanding of the influence of ligand promotion or inhibition of
weathering rates.
Research priorities for modelling biological weathering
Based on the preceding sections, we have identified five biological
processes that can be incorporated into models quantifying soil mineral
weathering rates, to make them more mechanistic and useful as predictive
tools:
exudation of LMW ligands promoting weathering;
nutrient uptake rates as a driver of weathering reactions;
the concentration effect of biofilms on weathering-promoting
ligands and protons;
the dependence of the above process on particular microbial and
plant assemblages, including mycorrhizal type;
the dependence of the above processes on carbon flux from
autotrophs, and the sensitivity of this to water and nutrient availability.
The stimulatory effect of particular LMW organic acids and siderophores on
soil mineral weathering rates is a function of both exudation rate and biological degradation rates of the same compounds. The chemical
composition of soil water DOC and exudates exerts considerable control on
the degree of stimulation, or, potentially, inhibition of weathering rates.
Modelling ligand-promoted dissolution as a function of total DOC without
consideration of DOC character may lead to inaccurate interpretations of
mineral dissolution rates derived from experiments with specific organic
species but should, with better data, open the door for more complex
descriptions of soil solutions and their effects on mineral weathering
rates.
Geochemical weathering models require the incorporation of mechanisms
(either through equilibrium equations or inhibitory factors) that allow the
build-up of weathering products to slow weathering rates. The treatment of
soil solution fluxes should allow for accumulation and removal of weathering
products in soil microenvironments (such as around mineral surfaces and
mycelia), as bulk soil solution data may not capture the concentration
gradients found around mineral surfaces. The observation, across a variety
of both empirical studies and modelling approaches, that nutrient uptake
into vegetation is a major driver of weathering rates should continue to
drive research into the effects of soil solution concentrations near mineral
surfaces, and their deviation from bulk soil solution, as a factor
controlling dissolution rates. Ongoing research into the extent and
chemistry of microbial biofilms in soils, aided by technological
developments in microprobes and spectroscopy, is giving an increased
understanding of their importance and extent in the soil for controlling the
solution chemistry at mineral surfaces, which may lead to incorporation into
models.
The dependence of biological weathering on particular microbial and plant
assemblages, in particular the mycorrhizal type, has not yet been determined and
requires further detailed studies of the specificity of
ectomycorrhiza–bacteria interactions and the physiological differences
between different bacteria and fungi in their ability to promote dissolution
of different minerals. A growing consensus on the importance of root length
density and hyphal length density as important explanatory factors governing
biological process rates may lead to increased inclusion of them as factors
or parameters in future models. Further information is also required on the
variation in carbon flux from autotrophs to different fungal and bacterial
components of biofilms in contact with different minerals and the
sensitivity of this carbon flux to differences in water and nutrient
availability. A major area of model development has been in global plant
productivity, not least because of its central role in the carbon cycle.
Advances in describing below-ground allocation (as opposed to above-ground)
have lagged far behind but are now increasing rapidly, and this should
provide valuable data to improve model descriptions of biological weathering
processes.
Conclusions
In this paper we attempt to outline the consequences of interactions between
minerals, microorganisms and plants at different spatial scales and to
review the influence of biological processes on mineral weathering within an
evolutionary context. The interaction of microorganisms with rocks and
minerals took place for 3.5 billion years before the appearance of the first
land plants and there is documented evidence that early microorganisms had
wide-ranging effects on both chemical and biological processes (Fig. 3),
including (a) the accumulation of oxygen in the atmosphere, and the
evolution of over two thirds of the minerals that exist today and (b) the
evolution of plastids through serial endosymbiosis. The subsequent evolution
of higher plants made possible by efficient photosynthesis and successive
increases in their size, nutrient acquisition and ability to colonise and
allocate photosynthetically derived carbon to mineral (and organic)
substrates, has enabled them to have increasing influence as biogeochemical
engineers (Fig. 3c–g). Microbial symbionts have played an integral part in
the evolution of plants and their ability to capture growth-limiting
nutrients such as N (Moreau et al., 2019). The influence of vegetation on
mineral substrates is almost axiomatic but quantification of the
contribution of plant-associated microorganisms to mineral weathering is
problematical for two reasons. Firstly, the ubiquitous distribution of
microorganisms, the fact that plants devoid of microorganisms do not exist
under natural conditions, means that plants need to be considered from a
more holistic perspective, as holobionts, together with the many different
microorganisms associated with them. Secondly, processes occurring at small spatial
scales are difficult to quantify and upscale to the catchment, ecosystem or
global scale. Although the combined effects of plants and their microbial
symbionts have quantifiable effects on mineral dissolution and capture of
nutrients, continued effort must be directed at elucidating the identity,
distribution and functional characteristics of these many different
microbial taxa. Sverdrup (2009) acknowledged the importance of
“biologically induced systemic effects” on weathering and concluded that
“the growth of the trees and forest growth represents the largest single
biological process that can affect weathering, followed closely by
decomposition of organic matter”. Boreal and temperate forest ecosystems
are characterised by ubiquitous symbiotic associations with ectomycorrhizal
fungi, and the central axiom of the current paradigm of ectomycorrhizal
functioning is that these systems have evolved to promote tree growth
through efficient uptake of nutrients, in particular through mobilisation of
N via decomposition of organic substrates (Lindahl and Tunlid, 2015;
Nicolás et al., 2019). Ectomycorrhizal fungi are therefore very likely to
influence mineral weathering directly or indirectly, and additional
information about their direct interactions with mineral substrates and
likely responses to different types of environmental stresses, including
those induced by forest management practices, is an important research
priority. Weathering of minerals is important not just with respect to the
sustainability of forestry. It is evident that the global weathering engine
has had long-term effects on atmospheric CO2 levels. Long-term
stabilisation of C, derived from the atmosphere, in organic and mineral
substrates, may take place through interactions involving glycoproteins,
melanin, extracellular polymeric substances, and formation of secondary
minerals and mineraloids. Better understanding of these processes may
facilitate improved forestry management practices that not only ensure
sustainable production of biomass but can also be integrated into new carbon
dioxide reduction technologies.
Data availability
Further details of data presented in Fig. 5 are available at 10.1111/1758-2229.12459 and sequences of the identified fungi are deposited in GenBank under the accession numbers KX451146 and KX451147.
Author contributions
RDF wrote most parts of the paper but with suggestions and inputs
from AR, KB and BL. NR, SB and SJK, in
particular, wrote most of the section on modelling, and EBB and HW provided substantial input to the section on stable isotopes. SM provided substantial input to Figs. 5 and 6. The work described in
Figs. 5 and 6 was carried out by SM and ZF with advice from
SJK. EBB carried out the stable isotope analyses in these
experiments.
Competing interests
The authors declare that they have no conflict of interest.
Special issue statement
This article is part of the special issue “Quantifying weathering rates for sustainable forestry (BG/SOIL
inter-journal SI)”. It is not associated with a conference.
Financial support
This research was supported by FORMAS, Swedish Research Council for Sustainable Development (grant nos. 2011-1691, 2014-01272 and 2017-00354).
Review statement
This paper was edited by Nobuhito Ohte and reviewed by three anonymous referees.
References
Ahmed, E. and Holmström, S. J. M.: Siderophores in
environmental research: roles and applications, Microb. Biotechnol., 7,
196–208, 2014.
Ahmed, E. and Holmstrom, S. J. M.: Microbe-mineral interactions: The impact
of surface attachment on mineral weathering and element selectivity by
microorganisms, Chem. Geol., 403, 13–23, 2015.Ahonen-Jonnarth, U., Van Hees, P. A. W., Lundstrom, U. S., and Finlay, R.
D.: Organic acids produced by mycorrhizal Pinus sylvestris exposed to elevated aluminium and
heavy metal concentrations, New Phytol., 146, 557–567, 2000.
Akselsson, C., Westling, O., Sverdrup, H., and Gundersen, P.: Nutrient and
carbon budgets in forest soils as decision support in sustainable forest
management, Forest Ecol. Manag., 238, 167–174, 2007.
Akselsson, C., Olsson, J., Belyazid, S., and Capell, R.: Can increased
weathering rates due to future warming compensate for base cation losses
following whole-tree harvesting in spruce forests?, Biogeochemistry, 128,
89–105, 2016.Akselsson, C., Belyazid, S., Stendahl, J., Finlay, R., Olsson, B. A., Erlandsson Lampa, M., Wallander, H., Gustafsson, J. P., and Bishop, K.: Weathering rates in Swedish forest soils, Biogeosciences, 16, 4429–4450, 10.5194/bg-16-4429-2019, 2019.Allen, J. F.: A proposal for formation of Archaean stromatolites before the
advent of oxygenic photosynthesis, Front. Microbiol., 7, 1784, 10.3389/fmicb.2016.01784, 2016.
Almeida, J. P., Rosenstock, N. P., Forsmark, B., Bergh, J., and Wallander, H.:
Ectomycorrhizal community composition and function in a spruce forest
transitioning between nitrogen and phosphorus limitation, Fungal. Ecol.,
40, 20–31, 2019.Andrews, J. A. and Schlesinger, W. H.: Soil CO2 dynamics,
acidification, and chemical weathering in a temperate forest with
experimental CO2 enrichment, Global Biogeochem. Cy., 15, 149–162, 2001.
Archibald, J. M.: Genomic perspectives on the birth and spread of plastids,
P. Natl. Acad. Sci. USA, 112, 10147–10153, 2015.
Averill, C., Dietze, M. C., and Bhatnagar, J. M.: Continental-scale nitrogen
pollution is shifting forest mycorrhizal associations and soil carbon
stocks, Glob. Change Biol., 24, 4544–4553, 2018.
Bahr, A., Ellstrom, M., Bergh, J., and Wallander, H.: Nitrogen leaching and
ectomycorrhizal nitrogen retention capacity in a Norway spruce forest
fertilized with nitrogen and phosphorus, Plant Soil, 390, 323–335, 2015.Balogh-Brunstad, Z., Kent Keller, C., Thomas Dickinson, J., Stevens, F., Li,
C. Y., and Bormann, B. T.: Biotite weathering and nutrient uptake by
ectomycorrhizal fungus, Suillus tomentosus, in liquid-culture experiments,
Geochim. Cosmochim. Ac., 72, 2601–2618, 2008.
Banfield, J. F., Barker, W. W., Welch, S. A., and Taunton, A.: Biological
impact on mineral dissolution: application of the lichen model to
understanding mineral weathering in the rhizosphere, P. Natl. Acad. Sci.
USA, 96, 3404–3411, 1999.Banwart, S. A., Berg, A., and Beerling, D. J.: Process-based modeling of
silicate mineral weathering responses to increasing atmospheric CO2 and
climate change, Global Biogeochem. Cy., 23, GB4013,
10.1029/2008GB003243, 2009.Beerling, D. J., Taylor, L. L., Bradshaw, C. D. C., Lunt, D. J., Valdes, P.
J., Banwart, S. A., Pagani, M., and Leake, J. R.: Ecosystem CO2
starvation and terrestrial silicate weathering: mechanisms and global-scale
quantification during the late Miocene, J. Ecol., 100, 31–41, 2012.
Beerling, D. J., Leake, J. R., Long, S. P., Scholes, J. D., Ton, J., Nelson,
P. N., Bird, M., Kantzas, E., Taylor, L. L., Sarkar, B., Kelland, M.,
DeLucia, E., Kantola, I., Muller, C., Rau, G. H., and Hansen, J.: Farming
with crops and rocks to address global climate, food and soil security, Nat.
Plants, 4, 138–147, 2018.
Bell, E. A., Boehnke, P., Harrison, T. M., and Mao, W. L.: Potentially
biogenic carbon preserved in a 4.1 billion-year-old zircon, P. Natl.
Acad. Sci. USA, 112, 14518–14521, 2015.Belyazid, S., Akselsson, C., and Zanchi, G.: Water limitation may restrict the positive effect of higher temperatures on weathering rates in forest soils, Biogeosciences Discuss., 10.5194/bg-2019-44, in review, 2019.Berner, R. A.: Paleoclimate – The rise of plants and their effect on
weathering and atmospheric CO2, Science, 276, 544–546, 1997.
Blum, J. D., Klaue, A., Nezat, C. A., Driscoll, C. T., Johnson, C. E.,
Siccama, T. G., Eagar, C., Fahey, T. J., and Likens, G. E.: Mycorrhizal
weathering of apatite as an important calcium source in base-poor forest
ecosystems, Nature, 417, 729–731, 2002.
Bolou-Bi, E. B., Vigier, N., Brenot, A., and Poszwa, A.: Magnesium isotope
compositions of natural reference materials, Geostand. Geoanal. Res., 33,
95–109, 2009.
Bolou-Bi, E. B., Vigier, N., Poszwa, A., Boudot, J. P., and Dambrine, E.:
Effects of biogeochemical processes on magnesium isotope variations in a
forested catchment in the Vosges Mountains (France), Geochim. Cosmochim. Ac., 87, 341–355, 2012.
Bonneville, S., Smits, M. M., Brown, A., Harrington, J., Leake, J. R.,
Brydson, R., and Benning, L. G.: Plant-driven fungal weathering: Early
stages of mineral alteration at the nanometer scale, Geology, 37, 615–618,
2009.
Bonneville, S., Morgan, D. J., Schmalenberger, A., Bray, A., Brown, A.,
Banwart, S. A., and Benning, L. G.: Tree-mycorrhiza symbiosis accelerate
mineral weathering: Evidences from nanometer-scale elemental fluxes at the
hypha–mineral interface, Geochim. Cosmochim. Ac., 75, 6988–7005, 2011.
Bonneville, S., Bray, A. W., and Benning, L. G.: Structural Fe(II) oxidation
in biotite by an ectomycorrhizal fungi drives mechanical forcing, Environ.
Sci. Technol., 50, 5589–5596, 2016.Borgeaud, S., Metzger, L. C., Scrignari, T., and Blokesch, M.: The type VI
secretion system of Vibrio cholerae fosters horizontal gene transfer, Science, 347, 63–67,
2015.
Brantley, S. L., Megonigal, J. P., Scatena, F. N., Balogh-Brunstad, Z.,
Barnes, R. T., Bruns, M. A., Van Cappellen, P., Dontsova, K., Hartnett, H.
E., Hartshorn, A. S., Heimsath, A., Herndon, E., Jin, L., Keller, C. K.,
Leake, J. R., McDowell, W. H., Meinzer, F. C., Mozdzer, T. J., Petsch, S.,
Pett-Ridge, J., Pregitzer, K. S., Raymond, P. A., Riebe, C. S., Shumaker,
K., Sutton-Grier, A., Walter, R., and Yoo, K.: Twelve testable hypotheses on
the geobiology of weathering, Geobiology, 9, 140–165, 2011.
Brocks, J. J., Logan, G. A., Buick, R., and Summons, R. E.: Archean
molecular fossils and the early rise of eukaryotes, Science, 285, 1033–1036,
1999.
Brown, G., Mitchell, D. T., and Stock, W. D.: Deposition of phosphorus in a
coastal Fynbos ecosystem of the south-western Cape, South Africa, J. Ecol.,
72, 547–551, 1984.Cailleau, G., Braissant, O., and Verrecchia, E. P.: Turning sunlight into stone: the oxalate-carbonate pathway in a tropical tree ecosystem, Biogeosciences, 8, 1755–1767, 10.5194/bg-8-1755-2011, 2011.
Cailleau, G., Mota, M., Bindschedler, S., Junier, P., and Verrecchia, E. P.:
Detection of active oxalate-carbonate pathway ecosystems in the Amazon
Basin: Global implications of a natural potential C sink, Catena, 116,
132–141, 2014.
Callot, G., Maurette, M., Pottier, L., and Dubois, A.: Biogenic Etching of
Microfractures in Amorphous and Crystalline Silicates, Nature, 328, 147–149,
1987.Calvaruso, C., Turpault, M-. P., Frey-Klett, P., Uroz, S., Pierret, M.-C.
Tosheva, Z., and Antoine, K.: Increase of apatite dissolution rate by Scots
pine roots associated or not with Burkholderia glathei PML1(12)Rp in open-system flow microcosms,
Geochim. Cosmochim. Ac., 106, 287–306, 2013.Chizhikova, N. P., Lessovaia, S. N., and Gorbushina, A. A.: Biogenic
Weathering of Mineral Substrates (Review), in: Biogenic-Abiogenic
Interactions in Natural and Anthropogenic Systems, edited by:
Frank-Kamenetskaya, O. V., Panova, E. G., and Vlasov, D. Y., Springer, Cham,
7–14, 10.1007/978-3-319-24987-2_2, 2016.
Clemmensen, K. E., Bahr, A., Ovaskainen, O., Dahlberg, A., Ekblad, A.,
Wallander, H., Stenlid, J., Finlay, R. D., Wardle, D. A., and Lindahl, B.
D.: Roots and associated fungi drive long-term carbon sequestration in
boreal forest, Science, 339, 1615–1618, 2013.
Cobert, F., Schmitt, A. D., Bourgeade, P., Labolle, F., Badot, P. M.,
Chabaux, F., and Stille, P.: Experimental identification of Ca isotopic
fractionations in higher plants, Geochim. Cosmochim. Ac., 75, 5467–5482,
2011.DasSarma, S. and Schwieterman, E. W.: Early evolution of purple retinal
pigments on Earth and implications for exoplanet biosignatures, Int. J.
Astrobiol., 1–10, 10.1017/S1473550418000423, 2018.
Deveau, A., Bonito, G., Uehling, J., Paoletti, M., Becker, M., Bindschedler,
S., Hacquard, S., Herve, V., Labbe, J., Lastovetsky, O. A., Mieszkin, S.,
Millet, L. J., Vajna, B., Junier, P., Bonfante, P., Krom, B. P., Olsson, S.,
van Elsas, J. D., and Wick, L. Y.: Bacterial-fungal interactions: ecology,
mechanisms and challenges, FEMS Microbiol. Rev., 42, 335–352, 2018.
Dijkstra, F. A. and Smits, M. M.: Tree species effects on calcium cycling:
the role of calcium uptake in deep soils, Ecosystems, 5, 385–398, 2002.Drever, J. I. and Stillings, L. L.: The role of organic acids in mineral
weathering, Coll. Surf. A, 120, 167–181, 10.1016/S0927-7757(96)03720-X,
1997.
Erlandsson, M., Oelkers, E. H., Bishop, K., Sverdrup, H., Belyazid, S.,
Ledesma, J. L. J., and Kohler, S. J.: Spatial and temporal variations of
base cation release from chemical weathering on a hillslope scale, Chem.
Geol., 441, 1–13, 2016.Fahad, Z. A., Bolou-Bi, E. B., Kohler, S. J., Finlay, R. D., and Mahmood,
S.: Fractionation and assimilation of Mg isotopes by fungi is species
dependent, Env. Microbiol. Rep., 8, 956–965, 10.1111/1758-2229.12459, 2016.
Ferris, F. G., Wiese, R. G., and Fyfe, W. S.: Precipitation of carbonate
minerals by microorganisms – Implications for silicate weathering and the
global carbon-dioxide budget, Geomicrobiol. J., 12, 1–13, 1994.Field, K. J., Cameron, D. D., Leake, J. R., Tille, S., Bidartondo, M. I.,
and Beerling, D. J.: Contrasting arbuscular mycorrhizal responses of vascular and non-vascular plants to a simulated Palaeozoic CO2 decline, 3, 835, 10.1038/ncomms1831, 2012.
Field, K. J., Davidson, S. J., Alghamadi, S. A., and Cameron, D. D.:
Magnitude, dynamics and control of carbon flow to mycorrhizas, in:
Mycorrhizal Mediation of Soil Fertility, Structure, and Carbon Storage,
edited by: Johnson, N. C., Gehring, C., and Jansa, J., Elsevier, Amsterdam,
375–393, ISBN 978-0-12-8043127, 2017.
Finlay, R. D. and Clemmensen, K. E.: Immobilization of carbon in
mycorrhizal mycelial biomass and secretions, in: Mycorrhizal Mediation of
Soil Fertility, Structure, and Carbon Storage, edited by: Johnson, N. C.,
Gehring, C., and Jansa, J.: Elsevier, Amsterdam, 413–440,
ISBN 978-0-12-8043127, 2017.
Finlay, R. D., Wallander, H., Smits, M., Holmstrom, S., Hees, P. V., Lian,
B., and Rosling, A.: The role of fungi in biogenic weathering in boreal forest
soils, Fung. Biol. Rev., 4, 101–106, 2009.
Flemming, H. C. and Wingender, J.: The biofilm matrix, Nat. Rev.
Microbiol., 8, 623–633, 2010.
Flemming, H. C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S. A., and
Kjelleberg, S.: Biofilms: an emergent form of bacterial life, Nat. Rev.
Microbiol., 14, 563–575, 2016.
Fomina, M., Burford, E. P., Hillier, S., Kierans, M., and Gadd, G. M.:
Rock-building fungi, Geomicrobiol. J., 27, 624–629, 2010.Futter, M. N., Klaminder, J., Lucas, R. W., Laudon, H., and Kohler, S. J.:
Uncertainty in silicate mineral weathering rate estimates: source
partitioning and policy implications, Environ. Res. Lett., 7, 024025, 10.1088/1748-9326/7/2/024025,
2012.
Gadd, G. M.: Metals, minerals and microbes: geomicrobiology and
bioremediation, Microbiology, 156, 609–643, 2010.
Gadd, G. M.: Microbial roles in mineral transformations and metal cycling in the Earth's critical zone, in: Molecular Environmental Soil Science. Progress in Soil Science, edited by: Xu J. and Sparks D.: Springer, Dordrecht, 115–165, ISBN 978-94-007-4176-8, 2013a.
Gadd, G. M.: Geomycology: Fungi as agents of biogeochemical change, Biology
and Environment, P. Roy. Irish Acad., 113b, 139–153, 2013b.
Gadd, G. M.: Fungi, rocks, and minerals, Elements, 13, 171–176, 2017.Gazzè, S. A., Saccone, L., Ragnarsdottir, K. V., Smits, M. M., Duran, A.
L., Leake, J. R., Banwart, S. A., and McMaster, T. J.: Nanoscale channels on
ectomycorrhizal-colonized chlorite: Evidence for plant-driven fungal
dissolution, J. Geophys. Res.-Biogeo., 117, G00n09, 10.1029/2012JG002016, 2012.
Gazzè, S. A., Saccone, L., Smits, M. M., Duran, A. L., Leake, J. R.,
Banwart, S. A., Ragnarsdottir, K. V., and McMaster, T. J.: Nanoscale
observations of extracellular polymeric substances deposition on
phyllosilicates by an ectomycorrhizal fungus, Geomicrobiol. J., 30, 721–730,
2013.
Gazze, S. A., Stack, A. G., Ragnarsdottir, K. V., and McMaster, T. J.:
Chlorite topography and dissolution of the interlayer studied with atomic
force microscopy, Am. Mineral., 99, 128–138, 2014.
Gleeson, D. B., Clipson, N., Melville, K., Gadd, G. M., and McDermott, F. P.:
Mineralogical control of fungal community structure in a weathered
pegmatitic granite, Microb. Ecol., 50, 360–368, 2005.
Gorbushina, A. A.: Life on the rocks, Env. Microbiol., 9, 1613–1631, 2007.
Goudie, A. S. and Viles, H. A.: Weathering and the global carbon cycle:
Geomorphological perspectives, Earth-Sci. Rev., 113, 59–71, 2012.
Griffiths, R. P., Baham, J. E., and Caldwell, B. A.: Soil solution chemistry of
ectomycorrhizal mats in forest soil, Soil Biol. Biochem., 26, 331–337, 1994.
Grube, M., Cernava, T., Soh, J., Fuchs, S., Aschenbrenner, I., Lassek, C.,
Wegner, U., Becher, D., Riedel, K., Sensen, C. W., and Berg, G.: Exploring
functional contexts of symbiotic sustain within lichen-associated bacteria
by comparative omics, ISME J., 9, 412–424, 2015.Guennoc, C. M., Rose, C., Labbe, J., and Deveau, A.: Bacterial biofilm
formation on the hyphae of ectomycorrhizal fungi: a widespread ability under
controls?, FEMS Microbiol. Ecol., 94, fiy093, 10.1093/femsec/fiy093,
2018.
Hartmann, J. and Moosdorf, N.: Chemical weathering rates of
silicate-dominated lithological classes and associated liberation rates of
phosphorus on the Japanese Archipelago – Implications for global scale
analysis, Chem. Geol., 287, 125–157, 2011.
Hazen, R. M., Papineau, D., Leeker, W. B., Downs, R. T., Ferry, J. M.,
McCoy, T. J., Sverjensky, D. A., and Yang, H. X.: Mineral evolution, Am.
Mineral., 93, 1693–1720, 2008.
Hibbett, D., Gilbert, L., and Donoghue, M.: Evolutionary instability of
ectomycorrhizal symbiosis in basidiomycetes, Nature, 407, 506–508, 2000.
Hindshaw, R. S., Reynolds, B. C., Wiederhold, J. G., Kretzschmar, R., and
Bourdon, B.: Calcium isotopes in a proglacial weathering environment: Damma
glacier, Switzerland, Geochim. Cosmochim. Ac., 75, 106–118, 2011.
Hodkinson, B. P., Gottel, N. R., Schadt, C. W., and Lutzoni, F.:
Photoautotrophic symbiont and geography are major factors affecting highly
structured and diverse bacterial communities in the lichen microbiome,
Environ. Microbiol., 14, 147–161, 2012.
Hoffland, E., Giesler, R., Jongmans, T., and van Breemen, N.: Increasing
feldspar tunneling by fungi across a north Sweden podzol chronosequence,
Ecosystems, 5, 11–22, 2002.
Hoffland, E., Giesler, R., Jongmans, A. G., and van Breemen, N.: Feldspar
tunneling by fungi along natural productivity gradients, Ecosystems, 6,
739–746, 2003.
Hoffland, E., Kuyper, T. W., Wallander, H., Plassard, C., Gorbushina, A. A.,
Haselwandter, K., Holmstrom, S., Landeweert, R., Lundstrom, U. S., Rosling,
A., Sen, R., Smits, M. M., van Hees, P. A., and van Breemen, N.: The role of
fungi in weathering, Front. Ecol. Environ., 2, 258–264, 2004.
Högberg, M. N. and Högberg, P.: Extramatrical ectomycorrhizal
mycelium contributes one-third of microbial biomass and produces, together
with associated roots, half the dissolved organic carbon in a forest soil,
New Phytol., 154, 791–795, 2002.
Högberg, P., Nordgren, A., Buchmann, N., Taylor, A. F. S., Ekblad, A.,
Högberg, M. N., Nyberg, G., Ottosson-Lofvenius, M., and Read, D. J.:
Large-scale forest girdling shows that current photosynthesis drives soil
respiration, Nature, 411, 789–792, 2001.
Holmden, C. and Belanger, N.: Ca isotope cycling in a forested ecosystem,
Geochim. Cosmochim. Ac., 74, 995–1015, 2010.
Holmstrom, S. J. M., Lundstrom, U. S., Finlay, R. D., and Van Hees, P. A.
W.: Siderophores in forest soil solution, Biogeochemistry, 71, 247–258,
2004.
Howard, R. J., Ferrari, M. A., Roach, D. H., and Money, N. P.: Penetration of
hard substrates by a fungus employing enormous turgor pressures, P. Natl.
Acad. Sci. USA, 88, 11281–11284, 1991.
Huang, K. J., Teng, F. Z., Wei, G. J., Ma, J. L., and Bao, Z. Y.:
Adsorption- and desorption-controlled magnesium isotope fractionation during
extreme weathering of basalt in Hainan Island, China, Earth Planet. Sc.
Lett., 359, 73–83, 2012.
Hutchens, E.: Microbial selectivity on mineral surfaces: possible
implications for weathering processes, Fung. Biol. Rev., 23, 115–121, 2010.Johansson, E. M., Fransson, P. M. A., Finlay, R. D., and van Hees, P. A. W.:
Quantitative analysis of soluble exudates produced by ectomycorrhizal roots
as a response to ambient and elevated CO2, Soil Biol. Biochem., 41,
1111–1116, 2009.
Jones, D. L., Nguyen, C., and Finlay, R. D.: Carbon flow in the rhizosphere:
carbon trading at the soil-root interface, Plant Soil, 321, 5–33, 2009.
Jongmans, A. G., van Breemen, N., Lundstrom, U., van Hees, P. A. W., Finlay,
R. D., Srinivasan, M., Unestam, T., Giesler, R., Melkerud, P. A., and
Olsson, M.: Rock-eating fungi, Nature, 389, 682–683, 1997.
Kalinowski, B. E., Liermann, L. J., Brantley, S. L., Barnes, A., and
Pantano, C. G.: X-ray photoelectron evidence for bacteria-enhanced
dissolution of hornblende, Geochim. Cosmochim. Ac., 64, 1331–1343, 2000.
Klaminder, J., Lucas, R. W., Futter, M. N., Bishop, K. H., Kohler, S. J.,
Egnell, G., and Laudon, H.: Silicate mineral weathering rate estimates: Are
they precise enough to be useful when predicting the recovery of nutrient
pools after harvesting?, Forest Ecol. Manag., 261, 1–9, 2011.
Koele, N., Dickie, I. A., Oleksyn, J., Richardson, S. J., and Reich, P. B.:
No globally consistent effect of ectomycorrhizal status on foliar traits,
New Phytol., 196, 845–852, 2012.
Koele, N., Dickie, I. A., Blum, J. D., Gleason, J. D., and de Graaf, L.:
Ecological significance of mineral weathering in ectomycorrhizal and
arbuscular mycorrhizal ecosystems from a field-based comparison, Soil Biol.
Biochem., 69, 63–70, 2014.
Kohler, A., Kuo, A., Nagy, L. G., Morin, E., Barry, K. W., Buscot, F., Canback, B., Choi, C., Cichocki, N., Clum, A., Colpaert, J., Copeland, A., Costa, M. D., Dore, J., Floudas, D., Gay, G., Girlanda, M., Henrissat, B., Herrmann, S., Hess, J., Hogberg, N., Johansson, T., Khouja, H. R., LaButti, K., Lahrmann, U., Levasseur, A., Lindquist, E. A., Lipzen, A., Marmeisse, R., Martino, E., Murat, C., Ngan, C. Y., Nehls, U., Plett, J. M., Pringle, A., Ohm, R. A., Perotto, S., Peter, M., Riley, R., Rineau, F., Ruytinx, J., Salamov, A., Shah, F., Sun, H., Tarkka, M., Tritt, A., Veneault-Fourrey, C., Zuccaro, A., Tunlid, A., Grigoriev, I. V., Hibbett, D. S., Martin, F., and Mycorrhizal Genomics Initiative: Convergent
losses of decay mechanisms and rapid turnover of symbiosis genes in
mycorrhizal mutualists, Nat. Genet., 47, 410–415, 2015.
Kohler, P., Hartmann, J., and Wolf-Gladrow, D. A.: Geoengineering potential
of artificially enhanced silicate weathering of olivine, P. Natl. Acad.
Sci. USA, 107, 20228–20233, 2010.
Kraemer, S. M., Duckworth, O. W., Harrington, J. M., and Schenkeveld, W. D.
C.: Metallophores and trace metal bio-geochemistry, Aquat. Geochem., 21,
159–195, 2014.
Kronnäs, V., Akselsson, C., and Belyazid, S.: Dynamic
modelling of weathering rates – the benefit over steady-state modelling,
Soil, 5, 33–47, 2019.
Kump, L. R.: The rise of atmospheric oxygen, Nature, 451, 277–278, 2008.
Lambers, H., Raven, J. A., Shaver, G. R., and Smith, S. E.: Plant
nutrient-acquisition strategies change with soil age, Trends Ecol. Evol.,
23, 95–103, 2008.
Lambers, H., Mougel, C., Jaillard, B., and Hinsinger, P.: Plant-microbe-soil
interactions in the rhizosphere: an evolutionary perspective, Plant Soil,
321, 83–115, 2009.
Landeweert, R., Hofflund, E., Finlay, R. D., and van Breemen, N.: Linking
plants to rocks: Ectomycorrhizal fungi mobilize nutrients from minerals,
Trends Ecol. Evol., 16, 248–254, 2001.
Lawrence, C., Harden, J., and Maher, K.: Modeling the influence of organic
acids on soil weathering, Geochim. Cosmochim. Ac., 139, 487–507, 2014.
Leake, J. R. and Read, D. J.: Mycorrhizal symbioses and pedogenesis
throughout Earth's history, in: Mycorrhizal Mediation of Soil Fertility,
Structure, and Carbon Storage, edited by: Johnson, N. C., Gehring, C., and
Jansa, J.: Elsevier, Amsterdam, 9–33, ISBN 978-0-12-8043127, 2017.
Leake, J. R., Duran, A. L., Hardy, K. E., Johnson, I., Beerling, D. J.,
Banwart, S. A., and Smits, M. M.: Biological weathering in soil: the role of
symbiotic root-associated fungi biosensing minerals and directing
photosynthate-energy into grain-scale mineral weathering, Min. Mag., 72,
85–89, 2008.
Li, Z. B., Liu, L. W., Chen, J., and Teng, H. H.: Cellular dissolution at
hypha- and spore- mineral interfaces revealing unrecognized mechanisms and
scales of fungal weathering, Geology, 44, 319–322, 2016.Lian, B., Wang, B., Pan, M., Liu, C. Q., and Teng, H. H.: Microbial release
of potassium from K-bearing minerals by thermophilic fungus Aspergillus fumigatus, Geochim.
Cosmochim. Ac., 72, 87–98, 2008.
Lian, B., Chen, Y., and Tang, Y. A.: Microbes on Carbonate Rocks and
Pedogenesis in Karst Regions, J. Earth Sci.-China, 21, 293–296, 2010.
Lian, B., Yuan, D. X., and Liu, Z. H.: Effect of microbes on karstification
in karst ecosystems, Chinese Sci. Bull., 56, 3743–3747, 2011.
Lindahl, B. D. and Tunlid, A.: Ectomycorrhizal fungi – potential organic
matter decomposers, yet not saprotrophs, New Phytol., 205, 1443–1447, 2015.
Lindahl, B. D., Ihrmark, K., Boberg, J., Trumbore, S. E., Hogberg, P.,
Stenlid, J., and Finlay, R. D.: Spatial separation of litter decomposition
and mycorrhizal nitrogen uptake in a boreal forest, New Phytol., 173,
611–620, 2007.Liu, H. L. and Lian, B.: Quantitative evaluation of different fractions of
extracellular polymeric substances derived from Paenibacillus mucilaginosus against the toxicity of
gold ions, Coll. Surf. B, 175, 195–201, 2019.Liu, Y. P., Sun, Q. B., Li, J., and Lian, B.: Bacterial diversity among the
fruit bodies of ectomycorrhizal and saprophytic fungi and their
corresponding hyphosphere soils, Sci. Rep., 8, 11672, 10.1038/s41598-018-30120-6, 2018.Luo, G. M., Ono, S. H., Beukes, N. J., Wang, D. T., Xie, S. C., and Summons,
R. E.: Rapid oxygenation of Earth's atmosphere 2.33 billion years ago, Sci.
Adv., 2, e1600134, 10.1126/sciadv.1600134, 2016.
Ma, J. F., Ryan, P. R., and Delhaize, E.: Aluminium tolerance in plants and
the complexing role of organic acids, Trends Plant Sci., 6, 273–278, 2001.
Maher, K.: The dependence of chemical weathering rates on fluid residence
time, Earth Planet. Sc. Lett., 294, 101–110, 2010.
Martin, F., Kohler, A., Murat, C., Veneault-Fourrey, C., and Hibbett, D. S.:
Unearthing the roots of ectomycorrhizal symbioses, Nat. Rev. Microbiol., 14, 760–773, 2016.
Martino, E., Perotto, S., Parsons, R., and Gadd, G. M.: Solubilization of
insoluble inorganic zinc compounds by ericoid mycorrhizal fungi derived from
heavy metal polluted sites, Soil Biol. Biochem., 35, 133–141, 2003.Marupakula, S., Mahmood, S., and Finlay, R. D.: Analysis of single root tip
microbiomes suggests that distinctive bacterial communities are selected by
Pinus sylvestris roots colonized by different ectomycorrhizal fungi, Env. Microbiol., 18,
1470–1483, 2016.Marupakula, S., Mahmood, S., Jernberg, J., Nallanchakravarthula, S., Fahad,
Z. A., and Finlay, R. D.: Bacterial microbiomes of individual
ectomycorrhizal Pinus sylvestris roots are shaped by soil horizon and differentially
sensitive to nitrogen addition, Env. Microbiol., 19, 4736–4753, 2017.
Mavromatis, V., Prokushkin, A. S., Pokrovsky, O. S., Viers, J., and Korets,
M. A.: Magnesium isotopes in permafrost-dominated Central Siberian larch
forest watersheds, Geochim. Cosmochim. Ac., 147, 76–89, 2014.
McLoughlin, N., Staudigel, H., Furnes, H., Eickmann, B., and Ivarsson, M.:
Mechanisms of microtunneling in rock substrates: distinguishing endolithic
biosignatures from abiotic microtunnels, Geobiology, 8, 245–255, 2010.
McMaster, T. J.: Atomic Force Microscopy of the fungi-mineral interface:
applications in mineral dissolution, weathering and biogeochemistry, Curr.
Opin. Biotech., 23, 562–569, 2012.
Mitchell, A. C., Lafreniere, M. J., Skidmore, M. L., and Boyd, E. S.:
Influence of bedrock mineral composition on microbial diversity in a
subglacial environment, Geology, 41, 855–858, 2013.
Moldan, F., Stadmark, J., Fölster, J., Jutterström, S., Futter, M.
N., Cosby, B. J., and Wright, R. F.: Consequences of intensive forest
harvesting on the recovery of Swedish lakes from acidification and on
critical load exceedances, Sci. Total Environ., 603, 562–569, 2017.
Montross, S. N., Skidmore, M., Tranter, M., Kivimaki, A. L., and Parkes, R. J.:
A microbial driver of chemical weathering in glaciated systems, Geology, 41,
215–218, 2013.
Moreau, D., Bardgett, R. D., Finlay, R. D., Jones, D. L., and Philippot, L.:
A plant perspective on nitrogen cycling in the rhizosphere, Funct. Ecol.,
33, 540–552, 2019.
Morris, J. L., Leake, J. R., Stein, W. E., Berry, C. M., Marshall, J. E. A.,
Wellman, C. H., Milton, A., Hillier, S., Mannolini, F., Quirk, J., and
Beerling, D. J.: Investigating Devonian trees as geoengineers of past
climates: linking palaeosols to palaeobotany and experimental geobiology,
Palaeontology, 58, 787–801, 2015.
Neaman, A., Chorover, J., and Brantley, S. L.: Effects of organic ligands on
granite dissolution in batch experiments at pH 6, Amer. J. Sci., 306, 451–473, 2006.
Nicolás, C., Martin-Bertelsen, T., Floudas, D., Bentzer, J., Smits, M.,
Johansson, T., Troein, C., Persson, P., and Tunlid, A.: The soil organic
matter decomposition mechanisms in ectomycorrhizal fungi are tuned for
liberating soil organic nitrogen, ISME J., 13, 977–988, 2019.
Ochs, M.: Influence of humified and non-humified natural organic compounds
on mineral dissolution, Chem. Geol., 132, 119–124, 1996.
Opfergelt, S., Burton, K. W., Georg, R. B., West, A. J., Guicharnaud, R. A.,
Sigfusson, B., Siebert, C., Gislason, S. R., and Halliday, A. N.: Magnesium
retention on the soil exchange complex controlling Mg isotope variations in
soils, soil solutions and vegetation in volcanic soils, Iceland, Geochim. Cosmochim. Ac., 125, 110–130, 2014.Pagani, M., Caldeira, K., Berner, R., and Beerling, D. J.: The role of
terrestrial plants in limiting atmospheric CO2 decline over the past 24
million years, Nature, 460, 85–94, 2009.
Page, B. D., Bullen, T. D., and Mitchell, M. J.: Influences of calcium
availability and tree species on Ca isotope fractionation in soil and
vegetation, Biogeochemistry, 88, 1–13, 2008.Paris, F., Bonnaud, P., Ranger, J., and Lapeyrie F.: In vitro weathering of
phlogopite by ectomycorrhizal fungi. I. Effect of K+ and Mg2+
deficiency on phyllosilicate evolution, Plant Soil, 177, 191–201, 1995.Paris, F., Botton, B., and Lapeyrie, F.: In vitro weathering of phlogopite by
ectomycorrhizal fungi. 2. Effect of K+ and Mg2+ deficiency and N
sources on accumulation of oxalate and H+, Plant Soil, 179, 141–50,
1996.
Perakis, S. S. and Pett-Ridge, J. C.: Nitrogen-fixing red alder trees tap
rock-derived nutrients, P. Natl. Acad. Sci. USA, 116, 5009–5014, 2019.Phelan, J., Belyazid, S., Kurz, D., Guthrie, S., Cajka, J., Sverdrup, H.,
and Waite, R.: Estimation of soil base cation weathering rates with the
PROFILE model to determine critical loads of acidity for forested ecosystems
in Pennsylvania, USA: Pilot application of a potential national
methodology, Water Air Soil Poll., 225, 2109,
10.1007/s11270-014-2109-4, 2014.
Philippot, L., Raaijmakers, J. M., Lemanceau, P., and van der Putten, W. H.:
Going back to the roots: the microbial ecology of the rhizosphere, Nat. Rev.
Microbiol., 11, 789–799, 2013.
Pogge von Strandmann, P. A. E., Burton, K. W., James, R. H., van Calsteren,
P., Gislason, S. R., and Sigfusson, B.: The influence of weathering
processes on riverine magnesium isotopes in a basaltic terrain, Earth
Planet. Sc. Lett., 276, 187–197, 2008.
Povak, N. A., Hessburg, P. F., McDonnell, T. C., Reynolds, K. M., Sullivan,
T. J., Salter, R. B., and Cosby, B. J.: Machine learning and linear regression
models to predict catchment-level base cation weathering rates across the
southern Appalachian Mountain region, USA, Water Resour. Res., 50,
2798–2814, 2014.Price, J. R., Peresolak, K., Brice, R. L., and Tefend, K. S.: Temporal
variability in the chemical weathering of Ca2+-bearing phases in the
Loch Vale watershed, Colorado, USA: A mass-balance approach, Chem. Geol.,
342, 151–166, 2013.
Querejeta, J. I., Egerton-Warburton, L. M., and Allen, M. F.: Direct
nocturnal water transfer from oaks to their mycorrhizal symbionts during
severe soil drying, Oecologia, 134, 55–64, 2003.
Quirk, J., Beerling, D. J., Banwart, S. A., Kakonyi, G., Romero-Gonzalez, M.
E., and Leake, J. R.: Evolution of trees and mycorrhizal fungi intensifies
silicate mineral weathering, Biol. Lett., 8, 1006–1011, 2012.Quirk, J., Andrews, M. Y., Leake, J. R., Banwart, S. A., and Beerling, D.
J.: Ectomycorrhizal fungi and past high CO2 atmospheres enhance mineral
weathering through increased below-ground carbon-energy fluxes, Biol. Lett.,
10, 20140375, 10.1098/rsbl.2014.0375, 2014a.Quirk, J., Leake, J. R., Banwart, S. A., Taylor, L. L., and Beerling, D. J.: Weathering by tree-root-associating fungi diminishes under simulated Cenozoic atmospheric CO2 decline, Biogeosciences, 11, 321–331, 10.5194/bg-11-321-2014, 2014b.Quirk, J., Leake, J. R., Johnson, D. A., Taylor, L. L., Saccone, L., and
Beerling, D. J.: Constraining the role of early land plants in Palaeozoic
weathering and global cooling, P. Roy. Soc. B, 282,
20151115, 10.1098/rspb.2015.1115, 2015.
Redfield, G. W.: Atmospheric deposition of phosphorus to the everglades:
concepts, constraints and published deposition rates for ecosystem
management, Sci. World J., 2, 1843–1873, 2002.
Reichard, P. U., Kraemer, S. M., Frazier, S. W., and Kretzschmar, R.:
Goethite dissolution in the presence of phytosiderophores: Rates,
mechanisms, and the synergistic effect of oxalate, Plant Soil, 276, 115–132,
2005.
Remiszewski, K. A., Bryce, J. G., Fahnestock, M. F, Pettitt, E. A.,
Blichert-Toft, J., Vadeboncoeur, M. A., and Bailey, S. W.: Elemental and
isotopic perspectives on the impact of arbuscular mycorrhizal and
ectomycorrhizal fungi on mineral weathering across imposed geologic
gradients, Chem. Geol., 445, 164–171, 2016.
Retallack, G. J.: Early forest soils and their role in Devonian global
change, Science, 276, 583–585, 1997.Roelandt, C., Goddéris, Y., and Bonnet, M.: Coupled modeling of
biospheric and chemical weathering processes at the continental scale, Global
Biogeochem. Cy., 24, GB2004, 10.1029/2008GB003420, 2010.
Rosenstock, N. P., Berner, C., Smits, M. M., Kram, P., and Wallander, H.:
The role of phosphorus, magnesium and potassium availability in soil fungal
exploration of mineral nutrient sources in Norway spruce forests, New
Phytol., 211, 542–553, 2016.
Rosling, A., Lindahl, B. D., and Finlay, R. D.: Carbon allocation to
ectomycorrhizal roots and mycelium colonising different mineral substrates,
New Phytol., 162, 795–802, 2004.
Rosling, A., Roose, T., Herrmann, A. M., Davidson, F. A., Finlay, R. D., and
Gadd, G. M.: Approaches to modelling mineral weathering by fungi, Fung.
Biol. Rev., 23, 138–144, 2009.
Ryan, M. H., Tibbett, M., Edmonds-Tibbett, T., Suriyagoda, L. D. B.,
Lambers, H., Cawthray, G. R., and Pang, J.: Carbon trading for phosphorus
gain: the balance between rhizosphere carboxylates and arbuscular
mycorrhizal symbiosis in plant phosphorus acquisition, Plant Cell Environ.,
35, 2170–2180, 2012.Ryu, J. S., Jacobson, A. D., Holmden, C., Lundstrom, C., and Zhang, Z. F.:
The major ion, delta Ca-44/40, delta Ca-44/42, and delta Mg-26/24
geochemistry of granite weathering at pH =1 and T =25 degrees C: power-law
processes and the relative reactivity of minerals, Geochim. Cosmochim. Ac.,
75, 6004–6026, 2011.
Saccone, L., Gazze, S. A., Duran, A. L., Leake, J. R., Banwart, S. A.,
Ragnarsdottir, K. V., Smits, M. M., and McMaster, T. J.: High resolution
characterization of ectomycorrhizal fungal-mineral interactions in axenic
microcosm experiments, Biogeochemistry, 111, 411–425, 2012.Savage, V. J., Chopra, I., and O'Neill, A. J.: Staphylococcus aureus biofilms promote horizontal
transfer of antibiotic resistance, Antimicrob. Agents Ch., 57,
1968–1970, 2013.Schmalenberger, A., Duran, A. L., Bray, A. W., Bridge, J., Bonneville, S.,
Benning, L. G., Romero-Gonzalez, M. E., Leake, J. R., and Banwart, S. A.:
Oxalate secretion by ectomycorrhizal Paxillus involutus is mineral-specific and controls
calcium weathering from minerals, Sci. Rep., 5, 12187, 10.1038/srep12187, 2015.
Seiffert, F., Bandow, N., Bouehez, J., von Blanekenburg, F., and Gorbushina,
A. A.: Microbial colonization of bare rocks: laboratory biofilm enhances
mineral weathering, Proced. Earth Plan. Sc., 10, 123–129, 2014.
Shen, B., Jacobsen, B., Lee, C. T. A., Yin, Q. Z., and Morton, D. M.: The Mg
isotopic systematics of granitoids in continental arcs and implications for
the role of chemical weathering in crust formation, P. Natl. Acad. Sci.
USA, 106, 20652–20657, 2009.Sigurbjornsdottir, M. A., Andresson, O. S., and Vilhelmsson, O.: Analysis of
the Peltigera membranacea metagenome indicates that lichen-associated bacteria are involved in
phosphate solubilization, Microbiol.-SGM, 161, 989–996, 2015.
Simonsson, M., Bergholm, J., Olsson, B., von Brömssen, C., and
Öborn, I.: Estimating weathering rates using base cation budgets in a
Norway spruce stand on podzolised soil: Analysis of fluxes and
uncertainties, Forest Ecol. Manag., 340, 135–152, 2015.
Smith, S. E. and Read, D. J.: Mycorrhizal Symbiosis, 3rd ed.,
Academic Press, Amsterdam, London, 2008.
Smits, M. M.: Scale matters? Exploring the effect of scale on fungal-mineral
interactions, Fung. Biol. Rev., 23, 132–137, 2009.
Smits, M. M. and Wallander, H.: Role of mycorrhizal symbiosis in mineral
weathering and nutrient mining from soil parent material, in: Mycorrhizal
Mediation of Soil Fertility, Structure, and Carbon Storage, edited by:
Johnson, N. C., Gehring, C., and Jansa, J., Elsevier, Amsterdam, 35–46,
ISBN 978-0-12-8043127, 2017.
Smits, M. M., Hoffland, E., Jongmans, A. G., and van Breemen, N.:
Contribution of mineral tunneling to total feldspar weathering, Geoderma,
125, 59–69, 2005.
Smits, M. M., Bonneville, S., Haward, S., and Leake, J. R.: Ectomycorrhizal
weathering, a matter of scale?, Mineral. Mag., 72, 131–134, 2008.
Smits, M. M., Bonneville, S., Benning, L. G., Banwart, S. A., and Leake, J.
R.: Plant-driven weathering of apatite – the role of an ectomycorrhizal
fungus, Geobiology, 10, 445–456, 2012.
Smits, M. M., Johansson, L., and Wallander, H.: Soil fungi appear to have a
retarding rather than a stimulating role on soil apatite weathering, Plant
Soil., 385, 217–228, 2014.
Söderström, B. E.: Seasonal fluctuations of active fungal biomass in
horizons of a podzolized pine-forest soil in central Sweden, Soil Biol.
Biochem., 11, 149–154, 1979.
Sokolova, T. A., Tolpeshta, I. I., and Topunova, I. V.: Biotite weathering
in podzolic soil under conditions of a model field experiment, Euras. Soil
Sci., 43, 1150–1158, 2010.
Stendahl, J., Akselsson, C., Melkerud, P. A., and Belyazid, S.: Pedon-scale
silicate weathering: comparison of the PROFILE model and the depletion
method at 16 forest sites in Sweden, Geoderma, 211, 65–74, 2013.
Sterkenburg, E., Clemmensen, K. E., Ekblad, A., Finlay, R. D., and Lindahl,
B. D.: Contrasting effects of ectomycorrhizal fungi on early and late stage
decomposition in a boreal forest, ISME J., 12, 2187–2197, 2018.
Sun, Q., Li, J., Finlay, R. D., and Lian, B.: Oxalotrophic bacteria
assemblages in the ectomycorrhizosphere and their effects on oxalate
degradation and carbon fixation potential, Chem. Geol., 514, 54–65, 2019a.Sun, Q., Ziyu, F., Finlay, R. D., and Lian, B.: Transcriptome analysis
provides novel insights into the response of the ectomycorrhizal fungus
Amanita pantherina to weather K-containing feldspar and apatite, Appl. Environ. Microb.,
85, e00719-19, 10.1128/AEM.00719-19, 2019b.Sun, Q. B. and Lian, B.: The different roles of Aspergillus nidulans carbonic anhydrases in
wollastonite weathering accompanied by carbonation, Geochim. Cosmochim. Ac., 244, 437–450, 2019.
Sun, Y. P., Unestam, T., Lucas, S. D., Johanson, K. J., Kenne, L., and
Finlay, R.: Exudation-reabsorption in a mycorrhizal fungus, the dynamic
interface for interaction with soil and soil microorganisms, Mycorrhiza, 9,
137–144, 1999.
Sverdrup, H.: Chemical weathering of soil minerals and the role of
biological processes, Fung. Biol. Rev., 23, 94–100, 2009.
Taylor, L., Banwart, S., Leake, J., and Beerling, D. J.: Modeling the
evolutionary rise of ectomycorrhiza on sub-surface weathering environments
and the geochemical carbon cycle, Am. J. Sci., 311, 369–403, 2011.
Taylor, L. L., Banwart, S. A., Valdes, P. J., Leake, J. R., and Beerling, D.
J.: Evaluating the effects of terrestrial ecosystems, climate and carbon
dioxide on weathering over geological time: a global-scale process-based
approach, Philos. T. R. Soc. B, 367, 565–582, 2012.
Taylor, L. L., Quirk, J., Thorley, R. M. S., Kharecha, P. A., Hansen, J.,
Ridgwell, A., Lomas, M. R., Banwart, S. A., and Beerling, D. J.: Enhanced
weathering strategies for stabilizing climate and averting ocean
acidification, Nat. Clim. Change, 6, 402–406, 2016.
Thorley, R. M. S., Taylor, L. L., Banwart, S. A., Leake, J. R., and
Beerling, D. J.: The role of forest trees and their mycorrhizal fungi in
carbonate rock weathering and its significance for global carbon cycling,
Plant Cell Environ., 38, 1947–1961, 2015.
Tipper, E. T., Gaillardet, J., Louvat, P., Capmas, F., and White, A. F.: Mg
isotope constraints on soil pore-fluid chemistry: Evidence from Santa Cruz,
California, Geochim. Cosmochim. Ac., 74, 3883–3896, 2010.
Toljander, J., Lindahl, B., Paul, L., Elfstrand, M., and Finlay, R. D..:
Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial
growth and community structure, FEMS Microbiol. Ecol., 61, 295–304, 2007.Tuason, M. M. S. and Arocena, J. M.: Calcium oxalate biomineralization by
Piloderma fallax in response to various levels of calcium and phosphorus, Appl. Environ.
Microb., 75, 7079–7085, 2009.
Turpault, M.-P., Nys, C., and Calvaruso, C.: Rhizosphere impact on the
dissolution of test minerals in a forest ecosystem, Geoderma, 153, 147–154,
2009.Uhlig, D., Schuessler, J. A., Bouchez, J., Dixon, J. L., and von Blanckenburg, F.: Quantifying nutrient uptake as driver of rock weathering in forest ecosystems by magnesium stable isotopes, Biogeosciences, 14, 3111–3128, 10.5194/bg-14-3111-2017, 2017.
Uroz, S., Oger, P., Lepleux, C., Collignon, C., Frey-Klett, P., and
Turpault, M. P.: Bacterial weathering and its contribution to nutrient
cycling in temperate forest ecosystems, Res. Microbiol., 162, 820–831, 2011.
Uroz, S., Turpault, M. P., Delaruelle, C., Mareschal, L., Pierrat, J. C.,
and Frey-Klett, P.: Minerals affect the specific diversity of forest soil
bacterial communities, Geomicrobiol. J., 29, 88–98, 2012.
Uroz, S., Kelly, L. C., Turpault, M. P., Lepleux, C., and Frey-Klett, P.:
The mineralosphere concept: Mineralogical control of the distribution and
function of mineral-associated bacterial communities, Trends Microbiol., 23,
751–762, 2015.Vaario, L. M., Pennanen, T., Lu, J. R., Palmen, J., Stenman, J., Leveinen,
J., Kilpelainen, P., and Kitunen, V.: Tricholoma matsutake can absorb and accumulate trace
elements directly from rock fragments in the shiro, Mycorrhiza, 25, 325–334,
2015.
van Breemen, N., Finlay, R., Lundstrom, U., Jongmans, A. G., Giesler, R.,
and Olsson, M.: Mycorrhizal weathering: A true case of mineral plant
nutrition?, Biogeochemistry, 49, 53–67, 2000.
Vandenkoornhuyse, P., Quaiser, A., Duhamel, M., Le Van, A., and Dufresne,
A.: The importance of the microbiome of the plant holobiont, New Phytol.,
206, 1196–1206, 2015.
van der Heijden, G., Bel, J., Craig, C. A., Midwood, A. J., Mareschal, L.,
Ranger, J., Dambrine, E., and Legout, A.: Measuring plant-available Mg, Ca,
and K pools in the soil-an isotopic dilution assay, ACS Earth Space Chem.,
2, 292–313, 2018.
van Hees, P. A. W., Vinogradoff, S. I., Edwards, A. C., Godbold, D. L., and
Jones, D. L.: Low molecular weight organic acid adsorption in forest soils:
effects on soil solution concentrations and biodegradation rates, Soil Biol.
Biochem., 35, 1015–1026, 2003.
van Hees, P. A. W., Jones, D. L., Finlay, R., Godbold, D. L., and
Lundström, U. S.: The carbon we do not see – the impact of low
molecular weight compounds on carbon dynamics and respiration in forest
soils: a review, Soil Biol. Biochem., 37, 1–13, 2005.van Hees, P. A. W., Rosling, A., Essen, S., Godbold, D. L., Jones, D. L.,
and Finlay, R. D.: Oxalate and ferricrocin exudation by the extramatrical
mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris, New Phytol., 169,
367–377, 2006.van Schöll, L., Hoffland, E., and van Breemen, N.:
Organic anion exudation by ectomycorrhizal fungi and Pinus sylvestris in response to
nutrient deficiencies, New Phytol., 170, 153–163, 2006a.
van Schöll, L., Smits, M. M., and Hoffland, E.:
Ectomycorrhizal weathering of the soil minerals muscovite and hornblende,
New Phytol., 171, 805–814, 2006b.
Verrecchia, E. P, Braissant, O., and Cailleau, G.: The oxalate-carbonate
pathway in soil carbon storage: the role of fungi and oxalotrophic bacteria,
in: Fungi in Biogeochemical Cycles, edited by: Gadd, G. M., Cambridge
University Press, Cambridge, 289–310, 2006.
Wallander, H., Johansson, L., and Pallon, J.: PIXE analysis to estimate the
elemental composition of ectomycorrhizal rhizomorphs grown in contact with
different minerals in forest soil, FEMS Microbiol. Ecol., 39, 147–156, 2002.
Wallander, H., Hagerberg, D., and Aberg, G.: Uptake of Sr-87 from microcline
and biotite by ectomycorrhizal fungi in a Norway spruce forest, Soil Biol.
Biochem., 38, 2487–2490, 2006.Wang, W. Y., Lian, B., and Pan, L.: An RNA-sequencing study of the genes and
metabolic pathways involved in Aspergillus niger weathering of potassium feldspar,
Geomicrobiol. J., 32, 689–700, 2015.
Watmough, S. A. and Dillon, P. J.: Mycorrhizal weathering in base-poor
forests, Nature, 423, 823–824, 2003.
Wilcke, W., Velescu, A., Leimer, S., Bigalke, M., Boy, J., and Valarezo, C.:
Biological versus geochemical control and environmental change drivers of
the base metal budgets of a tropical montane forest in Ecuador during 15
years, Biogeochemistry, 136, 167–189, 2017.
Wild, B., Imfeld, G., Guyot, F., and Daval, D.: Early stages of bacterial
community adaptation to silicate aging, Geology, 46, 555–558, 2018.
Wild, B., Daval, D., Beaulieu, E., Pierret, M.-C., Viville, D., and Imfeld,
G.: In-situ dissolution rates of silicate minerals and associated bacterial
communities in the critical zone (Strengbach catchment, France), Geochim. Cosmochim. Ac., 249, 95–120, 2019.
Wimpenny, J., Gislason, S. R., James, R. H., Gannoun, A., Pogge Von
Strandmann, P. A. E., and Burton, K. W.: The behaviour of Li and Mg isotopes
during primary phase dissolution and secondary mineral formation in basalt,
Geochim. Cosmochim. Ac., 74, 5259–5279, 2010.Winnick, M. J. and Maher, K.: Relationships between CO2, thermodynamic
limits on silicate weathering, and the strength of the silicate weathering
feedback, Earth Planet. Sc. Lett., 485, 111–120, 2018.Xiao, B., Lian, B., Sun, L. L., and Shao, W. L.: Gene transcription response
to weathering of K-bearing minerals by Aspergillus fumigatus, Chem. Geol., 306–307, 1–9, 10.1080/01490451.2014.884195, 2012.Xiao, L. L., Hao, J. C, Wang, W. Y., Lian, B., Shang, G. D., Yang, Y. W,
Liu, C. Q., and Wang, S. J.: The up-regulation of carbonic anhydrase genes of
Bacillus mucilaginosus under soluble Ca2+ deficiency and the heterologously expressed enzyme
promotes calcite dissolution, Geomicrobiol. J., 31, 632–641, 2014.Xiao, L. L., Lian, B., Hao, J. C., Liu, C. Q., and Wang, S. J.: Effect of
carbonic anhydrase on silicate weathering and carbonate formation at present
day CO2 concentrations compared to primordial values, Sci. Rep., 5,
7733, 10.1038/srep07733, 2015.
Xiao, L. L., Sun, Q. B., Yuan, H. T., and Lian, B.: A practical soil
management to improve soil quality by applying mineral organic fertilizer,
Acta Geochim., 36, 198–204, 2017.
Zetterberg, T., Olsson, B.A., Löfgren, S., Hyvönen, R., and
Brandtberg, P. O.: Long-term soil calcium depletion after conventional and
whole-tree harvest, Forest Ecol. Manag., 369, 102–115, 2016.
Zhang, L., Fan, J., Ding, X., He, X., Zhang, F., and Feng, G.: Hyphosphere
interactions between an arbuscular mycorrhizal fungus and a phosphate
solubilizing bacterium promote phytate mineralization in soil, Soil Biol.
Biochem., 74, 177–183, 2014.
Zhang, L., Xu, M., Liu, Y., Zhang, F., Hodge, A., and Feng. G.: Carbon and
phosphorus exchange may enable cooperation between an arbuscular mycorrhizal
fungus and a phosphate-solubilizing bacterium, New Phytol., 210, 1022–1032,
2016.
Zimorski, V., Ku, C., Martin, W. F., and Gould, S.B.: Endosymbiotic theory
for organelle origins, Curr. Opin. Microbiol., 22, 38–48, 2014.