In this study the organic matter (OM) in several permafrost cores from Bol'shoy Lyakhovsky Island in NE Siberia was investigated. In the context of the observed global warming the aim was to evaluate the potential of freeze-locked OM from different depositional ages to act as a substrate provider for microbial production of greenhouse gases from thawing permafrost. To assess this potential, the concentrations of free and bound acetate, which form an appropriate substrate for methanogenesis, were determined. The largest free-acetate (in pore water) and bound-acetate (organic-matrix-linked) substrate pools were present in interstadial marine isotope stage (MIS) 3 and stadial MIS 4 Yedoma permafrost deposits. In contrast, deposits from the last interglacial MIS 5e (Eemian) contained only a small pool of substrates. The Holocene (MIS 1) deposits revealed a significant bound-acetate pool, representing a future substrate potential upon release during OM degradation. Additionally, pyrolysis experiments on the OM allocated an increased aliphatic character to the MIS 3 and 4 Late Pleistocene deposits, which might indicate less decomposed and presumably more easily degradable OM. Biomarkers for past microbial communities, including those for methanogenic archaea, also showed the highest abundance during MIS 3 and 4, which indicated OM-stimulated microbial degradation and presumably greenhouse gas production during time of deposition. On a broader perspective, Arctic warming will increase and deepen permafrost thaw and favor substrate availability from older freeze-locked permafrost deposits. Thus, the Yedoma deposits especially showed a high potential for providing substrates relevant for microbial greenhouse gas production.
The northern areas of the Eurasian landmass are underlain by permafrost,
which is defined as ground that remains colder than 0
NE Siberian permafrost formation had already started in the late Pliocene,
e.g., at today's coasts and islands along the Dmitry Laptev Strait
(Arkhangelov et al., 1996). These deposits provide a unique
paleoenvironmental archive with stratigraphic patterns of long-lasting
accumulation periods of permafrost during glacial periods, as well as
permafrost degradation features during interglacial periods (Andreev et al.,
2004, 2009; Wetterich et al., 2009, 2011). Permafrost deposits were
accumulated under continental cold climate conditions, accompanied by
syngenetic ice-wedge growth (Wetterich et al., 2011) during glacial periods,
e.g., the middle Pleistocene (Saalian) and Late Pleistocene (Weichselian;
Yedoma deposits) (Andreev et al., 2004; Schirrmeister et al., 2013). In
contrast, during the Eemian (MIS 5e) and Holocene interglacial periods,
extensive thawing of ice wedges and permafrost deposits led to the formation
of thermokarst depressions, as well as of thermo-erosional valleys and small
rivers (Andreev et al., 2004; Ilyashuk et al., 2006; Wetterich et al.,
2009). According to pollen and insect data, the climate of the Eemian
resulted in an open grass and grass–sedge tundra similar to the modern
situation (Kienast et al., 2008). The mid-Eemian environment was
characterized by 4–5
These described environmental changes are expected to have a significant impact, not only on the amount, but also on the composition of the accumulated OM (Strauss et al., 2015; Stapel et al., 2016). After thawing, compositional differences in the formerly freeze-locked OM might strongly affect OM biodegradability and therefore the microbial production of greenhouse gases. To obtain deeper insights into the potential of permafrost OM from different ages to act as a substrate provider for intense microbial degradation, we examined characteristic OM parameters and exemplarily low-molecular-weight organic acid (LMWOA) concentrations. LMWOAs such as acetate are important and easily convertible substrates for microbial metabolism (Ganzert et al., 2007). Acetate is a well-known substrate for methanogenesis (Chin and Conrad, 1995). Thus, acetate concentrations provide valuable information on the greenhouse gas production potential of the respective OM (Stapel et al., 2016). On the one hand, acetate can be dissolved in pore water and cryostructures (e.g., segregated ice) of permafrost deposits. This acetate represents a free-substrate pool, which is directly bioavailable for microorganisms. On the other hand, acetate can be bound to the organic matrix (e.g., by ester linkage) forming a future substrate pool upon liberation via geochemical or microbial alteration of the OM (Glombitza et al., 2009a, b; Stapel et al., 2016).
In addition, microbial biomarkers such as phospholipid fatty acids (PLFAs) and glycerol dialkyl glycerol tetraethers (GDGTs) were analyzed to examine the interaction of present and past microbial communities with the OM accumulated in the past. Phospholipid esters are essential membrane components of living bacterial cells (Zelles, 1999) and are hydrolyzed rapidly after cell death (White et al., 1979; Logemann et al., 2011). Therefore, their fatty acid side chain inventories (PLFAs) are used as an indicator for viable microorganisms in sediments (Haack et al., 1994; Bischoff et al., 2013). In contrast, biomarkers such as GDGTs and archaeol represent membrane lipids of dead microbial biomass since they are already partly degraded as indicated by the loss of their head groups (Pease et al., 1998). While archaeol and GDGTs with isoprenoid tetraether bridges (isoGDGTs) represent archaeal biomass, GDGTs with branched tetraether bridges (brGDGTs) derive from bacteria (Weijers et al., 2006a, b). However, it should be mentioned that the brGDGT biomarkers only represent part of the bacterial community (Weijers et al., 2006a, b; Schouten et al., 2013), while the archaeal markers cover most of the past archaeal community (Pancost et al., 2001; Koga and Morii, 2006). In permafrost regions and peatlands archaeol is used as a biomarker for methanogenic archaea (Bischoff et al., 2013; Pancost et al., 2011).
The feedback between climate warming and microbial greenhouse gas generation from thawing permafrost is a topic of large global interest and intensive scientific debate (Zimov et al., 2006; Koven et al., 2011; Schuur et al., 2015). In this context the contribution from thawing OM of different depositional ages to the carbon–climate feedback cycle is still unclear. In order to learn more about this interrelation, we conducted a study on Bol'shoy Lyakhovsky Island in the Laptev Sea (NE Siberia). Samples from this region provided an excellent opportunity to investigate permafrost OM that was deposited from the last interglacial to the Holocene. The aims of our study were (1) to assess and compare the stored OM potential for microbial greenhouse gas production in permafrost deposits from different glacial and interglacial periods and (2) to assign this substrate potential to characteristic OM parameters and depositional paleoenvironmental conditions.
Bol'shoy Lyakhovsky Island is located between the Laptev and
East Siberian seas as the southernmost part of the New Siberian Archipelago
(Fig. 1a). During Pleistocene periods of low sea level the island was part
of west Beringia, an unglaciated landmass stretching from NE Siberia to
Alaska (Hubberten et al., 2004; Andreev et al., 2009). The area is part of
the northern tundra zone with an active layer (AL) thickness of 30–40
The field work was conducted in April 2014 as part of the joint
Russian–German research project CARBOPERM (Schwamborn and Wetterich, 2015).
Four cores were drilled using a KMB-3-15M (rotary) drill rig. The drilled
core segments were kept frozen and transported in the frozen state for
further processing to Potsdam, Germany. In our home laboratory sampling was
conducted in a climate chamber at
Schematic overview of assigned ages of the core material drilled on Bol'shoy Lyakhovsky Island showing the different cores with their drilling positions in relation to different age periods (interval names, marine isotope stages (MIS) and Russian terminology (RT) for the respective time periods). The age assignment is based on information obtained from Andreev et al. (2004, 2009) and Wetterich et al. (2009, 2014).
Cores are described stratigraphically from younger to older deposits. Core
L14-05 (Fig. 1c) is 7.89
Core L14-02 (Fig. 1c) is 20.02
The upper 4.90
Core L14-04 (Fig. 1c) is 8.10
After freeze-drying and grinding, samples for TOC analysis were decalcified
with 0.1
After slow thawing of a subset of the frozen samples at about 4
Approximately 30–50
After asphaltene precipitation the low polar lipid fraction was separated into aliphatic, aromatic, and hetero-compound (containing nitrogen, sulfur, and oxygen components; NSO) fractions using a medium-pressure liquid chromatography system (Radke et al., 1980). An aliquot of the NSO fraction was investigated for tetraether lipids (GDGTs) and archaeol using a Shimadzu LC20AD HPLC instrument coupled to a Finnigan TSQ 7000 triple quadrupole MS instrument with an atmospheric pressure chemical ionization interface. An external archaeol standard was used for quantification. Details on instrument settings are described in Stapel et al. (2016). The branched vs. isoprenoid tetraether (BIT) index was calculated after Hopmans et al. (2004). The data on individual GDGTs are provided in the Supplement (Tables S1 and S2). For GDGT compound structures see Schouten et al. (2013).
For statistical analysis of the measured parameters, the Pearson correlation
coefficient (
Bio- and geochemical parameters of permafrost cores L14-05,
L14-02, L14-03, and L14-04 from Bol'shoy Lyakhovsky Island,
northern Siberia, presented with respect to core depth (left axis) as well
as stratigraphic and age units (right column). The vertical profiles show
(note partly different
Triangular plots derived from organic matter (OM) open-system
pyrolysis.
Characteristic OM parameters (TOC, TOC
In the ALs TOC concentrations were above 2
In the MIS 1 permafrost section of core L14-05, the TOC, TOC
MIS 3 comprised the core sections MIS 3-1 from core L14-05 as well as MIS 3-2
and MIS 3-3 from core L14-02 (Table 1, Fig. 2). Overall, the TOC
contents and TOC
MIS 4 comprised the core sections MIS 4-1 from core L14-03 and MIS 4-2 from
core L14-04. The TOC contents and TOC
In the MIS 5e (Eemian) interval from core L14-04, TOC contents and TOC
Results provided by open-system pyrolysis experiments on 17 representative samples (high and low TOC) enabled a deeper insight into the OM characteristics. Figure 3a (after Eglinton et al., 1990) classifies the deposited OM into aliphatic-, aromatic-, or sulfur-rich OM. All samples from the Holocene (H1, H2, H3, H4, H5) and Eemian (E1, E2, E3) units and two samples from the LP unit (LP3, LP6) fell within the range of OM type III (terrestrial OM type). LP samples (LP4, LP5, LP7, LP8) corresponding to higher HI values showed a mixture of OM types III and II (increased aliphatic character). Two LP samples (LP1, LP2) and the AL sample, all displaying the highest HI values, fell within the range of OM type II. All samples, especially the samples from the Eemian (MIS 5e), showed only a very low abundance of sulfur compounds generated by pyrolysis, indicating sulfur-poor OM (2,3-dimethylthiophene).
Figure 3b (after Horsfield et al., 1989) suggests different aliphatic
characters for the selected samples, indicating an increasing aliphatic
character with higher HI and TOC. Samples from the Eemian unit (E1, E2, E3)
and the Holocene sample (H1) as well as two samples from the LP unit (LP3,
LP6) all with low HI (
When permafrost thaws, formerly freeze-locked OM becomes bioavailable again (Wagner et al., 2007; Lee et al., 2012). In order to assess the impact of this OM on future climate evolution it is of the utmost interest to learn more about the degradability of the thawing OM, especially with regard to its potential to release greenhouse gases. OM degradability in soils can be influenced by the molecular structure of the source OM and the decomposition processes that affected this material during deposition. Thereby, decomposition is affected by environmental factors (temperature, water saturation causing oxic or anoxic conditions, and adsorption onto the mineral soil matrix) and biological controls concerning the microbial ecosystem involved (Schmidt et al., 2011). In this paper the focus is placed on the OM composition and its specific characteristics. However, environmental and biological controls on OM degradation and accumulation are also considered.
Schematic summary compiling the assigned ages (time period and
marine isotope stage (MIS) classification) of the core material from
Bol'shoy Lyakhovsky Island based on Andreev et al. (2004, 2009) and
Wetterich et al. (2009, 2014), the paleoenvironmental information on
the different time intervals (
The composition of permafrost OM is mainly a mix of different terrestrial sources and the result of early diagenetic degradation processes during OM deposition in the past (White, 2013). We applied pyrolysis techniques (Rock-Eval pyrolysis and open-system pyrolysis GC-FID) to the OM to gain a deeper insight into the structural composition and to define specific characteristics for OM of different depositional ages.
The highest accumulation of OM, up to 4.9
In contrast, the low TOC concentrations and HI values of the Eemian samples (MIS 5e, Table 1) point to less OM accumulation and/or an increased level of OM decomposition. This could reflect the warmer and drier climate of the Eemian period in NE Siberia (Andreev et al., 2004; Wetterich et al., 2014, 2016), which might have supported intense aerobic microbial degradation of OM due to drier soil conditions (Andreev et al., 2009). The last interglacial was characterized by higher summer temperatures compared to the LP glacial period and even to the Holocene (Bond et al., 2001; Shackleton et al., 2003; Kienast et al., 2008, 2011) and was accompanied by permafrost thawing and draining, thermokarst formation, and thermal erosion (Table 2) (Andreev et al., 2009). The open-system pyrolysis data (Fig. 3) for the Eemian deposits (E1, E2, E3) showed a more pronounced type III OM and a less-aliphatic character compared to the Yedoma samples. Comparing the Eemian with the Holocene interglacial deposits (both are interpreted to have comparable vegetation – Kienast et al., 2008), the Holocene samples were characterized by higher TOC contents, HI values, and aliphatic proportions. This might indicate less-decomposed OM during deposition and therefore more favorable characteristics for OM degradation in future than for the Eemian deposits.
In addition to the environmental conditions in our study, the OM
characteristics might also have been influenced by the depositional
settings. Both the Holocene and Eemian OM were deposited in thermokarst lake
environments (Wetterich et al., 2009). Comparing the TOC contents from our
study with those from thermokarst lakes in the Kolyma region further to the
east (Peterse et al., 2014), it becomes clear that the Holocene and Eemian
deposits on Bol'shoy Lyakhovsky Island show much lower TOC
contents (Holocene: 0.21 to 1.81
In order to investigate whether the freeze-locked OM had already stimulated a diverse bacterial and archaeal community during deposition in the past, biomarkers for past microbial communities were examined. Intervals with increased abundance of biomarkers characteristic of methanogenic archaea are of particular interest. This will provide information on how the deposited OM of different ages had already stimulated microbial greenhouse gas production in the past, which will help to assess the potential of the OM for greenhouse gas production upon future permafrost thaw. Since past microbial biomarkers could also be a degradation product of the presently living microbial community, the Bol'shoy Lyakhovsky samples were also screened with regard to microbial life markers to compare both biomarker records.
As life markers we used phospholipids with ester bound fatty acids (PLFAs) since these bacterial cell membrane components are rapidly degraded after cell death (Logemann et al., 2011). In contrast, intact polar lipids with ether-bound moieties (diether side chain or tetraethers) have only a restricted potential to act as life markers for bacteria or archaea due to their significantly higher stability (Logemann et al., 2011). Thus, since microbial communities generally consist of both bacteria and archaea, we used the PLFAs here as a general indicator for intervals of increased present microbial life.
The detection of PLFA life markers indicated the occurrence of living bacterial communities in all investigated cores from Bol'shoy Lyakhovsky. While the PLFA signals were low in the permafrost sequences, all ALs contained higher concentrations of PLFAs (Fig. 2d). This indicates a larger microbial community in the surface layers and presumably also increased microbial activity, at least during the summer season. According to Knoblauch et al. (2013), permafrost surface layers contain a mix of newly produced and old OM; this OM can stimulate microbial activity during unfrozen periods. Signals of microbial life in permafrost deposits are strongly decreased compared to those seen in the AL. It has been suggested that the life marker signals in the permafrost section most likely represent living successors of the microbial community incorporated into the sediments during time of deposition (Bischoff et al., 2013). Thus, the permafrost preserved the microbial community of the past. Different studies have shown that the microbial cells in permafrost can be reactivated upon permafrost thaw, after which they are able to produce greenhouse gases (e.g., Knoblauch et al., 2013; Schuur et al., 2015; Treat et al., 2015; Walz et al., 2017).
GDGTs and archaeol represent past microbial biomass (Stapel et al., 2016). GDGTs and archaeol are the cores of former membrane lipids, which are already partly degraded as indicated by the loss of their head group moieties. However, the core lipids are very stable over geological timescales (Pease et al., 1998; Schouten et al., 2013) and can be found in many different habitats (Bischoff et al., 2013; Schouten et al., 2013). Past bacterial markers (brGDGTs – Weijers et al., 2006a, b) and archaeal markers (isoGDGTs and archaeol – Koga et al., 1993; Pancost et al., 2001) provide information on the abundance of a past microbial community and might provide indirect information about microbial activity during time of deposition. IsoGDGT-0 (no cyclopentyl rings in the tetraether alkyl chains) and archaeol are used as markers for methanogenic communities in permafrost and peatland environments (Pancost et al., 2011; Bischoff et al., 2014), whereas their relative proportion varies between different methanogenic genera (Koga and Mori, 2006). PLFA life marker profiles indicated abundant present microbial life only for the ALs and did not correlate with the past biomarkers. Thus, the data suggest that in the permafrost sequence the past markers represent a paleo-signal (Stapel et al., 2016).
The results on past bacterial and archaeal biomarkers (Fig. 2e to g) showed that intervals with increased concentrations often corresponded to increased OM contents (TOC, Fig. 2a) with higher aliphatic character (higher HI values). This could especially be observed in the Yedoma deposits with the core sections MIS 3-1 and 3-2 and the upper part of MIS 4-1 and 4-2 (Fig. 2c: LP1, LP2, LP4, and LP8). The archaeol profile (Fig. 2g) suggested the presence of methanogenic communities during these intervals and methane production from this kind of OM in the past. Thus, the microbial past markers indicate that the OM-rich Yedoma deposits supported an abundant microbial life including methanogenic archaea during time of deposition. Comparable trends (with some deviations when TOC contents are quite low) can be observed when relating the past biomarkers to gTOC (grams of TOC) (Fig. S1 in the Supplement).
A slight increase in permafrost temperatures is expected to influence not
only the soil-moisture content but also the abundance and diversity of the
microbial community (Wagner et al., 2007). Thus, intervals with increased
past biomarker concentrations in permafrost regions might reflect increased
soil moisture during time of deposition forming favorable living conditions
for anaerobic bacteria (Weijers et al., 2006a) and archaea (Wagner et al.,
2007). According to Wetterich et al. (2014), the MIS 3 interstadial optimum
occurred between 48 and 38
As outlined above, the Holocene (MIS 1) and Eemian (MIS 5e) successions in
this study were deposited in a thermokarst lake environment (Andreev et al.,
2004, 2009; Wetterich et al., 2009, 2014). Peterse et al. (2014) reported
much higher concentrations of brGDGTs (ranging between 7037 and 47 676
To assess the potential of the OM from different depositional ages to provide substrates for the production of greenhouse gases, acetate is used as an appropriate substrate for microbial metabolism (Ivarson and Stevenson, 1964; Sørensen and Paul, 1971; Sansone and Martens, 1981; Balba and Nedwell, 1982). Acetate is the terminal electron acceptor for methanogens in cold-temperate environments (Chin and Conrad, 1995; Wagner and Pfeiffer, 1997), especially for acetoclastic methanogens (Thauer, 1998). They are ubiquitous methanogenic archaea in anoxic environments and in permafrost sediments (Kobabe et al., 2004).
In this study two acetate pools were investigated: (1) the free-acetate pool
within the pore water, representing an easily and quickly accessible
substrate source for microbial metabolism, and (2) the bound-acetate
fraction, which is still linked to the OM. The latter constitutes a future
substrate source upon degradation (Glombitza et al., 2009b). The
concentrations of bound acetate (Fig. 2h) in the investigated samples
correlated well with the amount of TOC and also often with the HI values.
Overall, the largest future substrate potential for microbial turnover is
associated with MIS 3 (mean concentrations of
In the AL samples the very low concentrations of free acetate together with the elevated concentrations of PLFA life markers suggest a higher microbial consumption of free acetate by an active microbial community (Lee et al., 2012; Knoblauch et al., 2013; Stapel et al., 2016). This activity is most likely stimulated by, for example, warmer temperatures (thawing conditions) and the input of newly produced and old OM during the thawing period. AL deepening due to global warming especially increases the accessibility of formerly freeze-locked OM. This old OM has been reported to be particularly sensitive to temperature-induced microbial decomposition (Knorr et al., 2005; Davidson and Janssens, 2006) and, therefore, is considered to be an important substrate source for future microbial turnover.
In the present study, the highest PLFA concentration was detected in the AL of the core sequence containing MIS 3 deposits (core L14-02). This may reflect the high potential of the MIS 3 Yedoma OM to serve as a substrate provider for a living microbial community upon thaw. However, local environmental differences may also affect the PLFA concentration. For example, the core containing MIS 3 deposits was drilled on a stable tundra surface (core L14-02) with relatively stable AL conditions. In contrast, the other cores were either drilled in a geomorphologically dynamic terrace position with thermo-erosion (Schirrmeister et al., 2011a, b; Grosse et al., 2011) and a seasonal supply of sediment and water, or in a drained and refrozen Holocene thermokarst basin (core L14-05), which is characterized by lower ice contents and shallower ALs (Schwamborn and Wetterich, 2015). Nevertheless, the increased PLFA concentrations in all ALs indicate, to a certain extent, that the permafrost OM, at least from MIS 3, 4, and 1, can serve as a good substrate provider in a future permafrost thawing scenario. For MIS 5e OM this could not be evaluated due to the lack of MIS 5e deposits with an AL on top.
In contrast to the bound-acetate concentrations, the free-acetate substrate
pool only partly correlated with the TOC contents in the individual cores
(in all cores:
Overall, the Yedoma deposits (MIS 3 and MIS 4) contain the largest free- and bound-acetate substrate pools (Fig. 2h, i). They are rich in OM and are characterized by the highest abundance of past microbial biomarkers, including those resembling methanogenic communities in wetlands (Fig. 2e to g). The Yedoma organic-rich material often shows high HI values, assigning an increased aliphatic character to this OM (Fig. 3a, b). Thus, in contrast to simply using the TOC content, the HI values seem to represent a promising parameter for assessing the potential of permafrost OM to act as appropriate source material for microbial OM degradation. OM with high HI is considered to contain a higher proportion of more easily degradable aliphatic molecular structures, whereas OM with a low HI contains a higher proportion of less easily degradable aromatic structures (Hedges et al., 2000).
Analog results were obtained for Yedoma deposits in a previous study on Buor
Khaya Peninsula about 400
The potential of the permafrost OM to provide organic substrates for microbial greenhouse gas production strongly varies within the investigated deposits from the Eemian to the present time and is mainly controlled by environmental and climatic conditions. Overall, the strongest present and future substrate potential appears to be stored within the Yedoma OM deposits from the last interstadial (MIS 3) and stadial (MIS 4) periods, which are characterized by increased HI values and a higher aliphatic character. Thus, this currently frozen Yedoma OM is likely to have a strong impact on the greenhouse-gas-driven climate–carbon feedback cycle upon thaw. In contrast, the interglacial periods (Holocene and especially Eemian) show lower substrate potentials, which might point to stronger microbial degradation during time of deposition. The Eemian deposits reveal both low present and low future substrate pools. However, the Holocene deposits at least contain a significant future substrate pool, which may become available when recycled in the AL.
Data are available at
The supplement related to this article is available online at:
JGS conducted subsampling of the core material; the laboratory analyses and data interpretations were guided by KM and BH. GS and LS planned and coordinated the fieldwork as well as drilled and processed the core material. JGS wrote the paper, which was commented on by all co-authors.
The authors declare that they have no conflict of interest.
This research was supported by the German Ministry of Education and Research as part of the bilateral CARBOPERM Project between Germany and Russia (grant no. 03G0836B). We thank all Russian and German participants of the drilling expedition, especially Mikhail N. Grigoriev (Melnikov Permafrost Institute, Yakutsk, Russia) for his leadership. We thank the three reviewers for their thoughtful and very constructive comments and suggestions on our paper. Furthermore, a previous version of the paper benefited from valuable comments and English language correction from Candace O'Connor (Fairbanks, Alaska, USA). The article processing charges for this open-access publication were covered by a Research Centre of the Helmholtz Association. Edited by: Jack Middelburg Reviewed by: R. Sparkes and two anonymous referees