Biogeosciences
www.biogeosciences.net
1726-4170
1726-4189
4
4
2007
10.5194/bg-4-613-2007
http://www.biogeosciences.net/4/613/2007/
http://www.biogeosciences.net/4/613/2007/bg-4-613-2007.html
http://www.biogeosciences.net/4/613/2007/bg-4-613-2007.pdf
613
626
2007-08-08
Different carbon isotope fractionation patterns during the development of phototrophic freshwater and marine biofilms
M. Staal
mstaal@bi.ku.dk
R. Thar
M. Kühl
M. C. M. van Loosdrecht
G. Wolf
J. F. C. de Brouwer
J. W. Rijstenbil
Department of Marine Microbiology, Netherlands Institute of Ecology – KNAW, P.O. Box 140, 4400 AC Yerseke, The Netherlands
Marine Biological Laboratory, Institute of Biology, University of Copenhagen, Strandpromenaden 5, 3000 Helsingør, Denmark
Department of Environmental Biotechnology, TU Delft, Julianalaan 67, 2628 BC Delft, The Netherlands
present address: Marine Biological Laboratory, Institute of Biology, University of Copenhagen, Strandpromenaden 5, 3000 Helsingør, Denmark
present address: AE3 Consultancy, Fuchsialaan 8, 4401HV Yerseke, The Netherlands
Natural phototrophic biofilms are influenced by a broad array of abiotic and
biotic factors and vary over temporal and spatial scales. Different
developmental stages can be distinguished and growth rates will vary due to
the thickening of the biofilm, which is expected to lead to a limitation of
light or mass transport. This study shows that variation in CO<sub>2(aq)</sub>
availability leads to a fractionation shift and thereby affects δ<sup>13</sup>C
signatures during biofilm development. For phototrophic freshwater
biofilms it was found that the δ<sup>13</sup>C value became less negative
with the thickening of the biofilm, while the opposite trend was found in
marine biofilms. Modeling and pH profiling indicated that the trend in the
freshwater system was caused by an increase in CO<sub>2(aq)</sub> limitation
resulting in an increase of HCO<sub>3</sub><sup>−</sup> as C-source. The opposite trend
in the marine system could be explained by a higher heterotrophic biomass
and activity causing a higher carbon recycling and thereby lower δ<sup>13</sup>C
values. We conclude that δ<sup>13</sup>C was more related to the
net areal photosynthesis rate and carbon recycling, rather than to the
growth rate of the biofilms.
Bade, D. L., Carpenter, S. R., Cole, J. J., Hanson, P. C., and Hesslein, R. H.: Controls of delta C-13-DIC in lakes: Geochemistry, lake metabolism, and morphometry, Limnnol. Oceanogr., 49, 1160–1172, 2004.
Biggs, B. J. F.: Patterns in benthic algae of streams, in: Algal Ecology: Freshwater Benthic Ecosystems, edited by: Stevenson, R. J., Bothwell, M. L., and Lowe, R. L., San Diego, Academic Press, 31–56, 1996.
Boschker, H. T. S.: Linking microbial community structure and functioning: stable isotope (13C) labeling in combination with PLFA analysis, in: Molecular Microbial Ecology Manual II, edited by: Kowalchuk, G. A., de Bruijn, F. J., Head, I. M., Akkermans, A. D., and van Elsas, J. D., Dordrecht, The Netherlands, Kluwer Academic Publishers, 1673–1688, 2004.
Boschker, H. T. S., Kromkamp, J. C., and Middelburg, J. J.: Biomarker and carbon isotopic constraints on bacterial and algal community structure and functioning in a turbid, tidal estuary, Limnnol. Oceanogr., 50, 70–80, 2005.
Bott, T. L.: Algae in microscopic food webs, in: Algal Ecology: Freshwater Benthic Ecosystems, edited by: Stevenson, R. J., Bothwell, M. L., and Lowe, R. L., San Diego, Academic Press, 574–609, 1996.
Cassar, N., Laws, E. A., Bidigare, R. R., and Popp, B. N.: Bicarbonate uptake by Southern Ocean phytoplankton, Global Geochem. Cy., 18, 1–10, 2004.
Charlebois, P. M. and Lamberti, G. A.: Invading crayfish in a Michigan stream: Direct and indirect effects on periphyton and macroinvertebrates, J. N. Am. Benthol. Soc., 15, 551–563, 1996.
Congestri, R., Cox, E. J., Cavacini, P., and Albertano, P.: Diatoms (Bacillariophyta) in phototrophic biofilms colonising an italian wastewater treatment plant, Diatom Res., 20, 241–255, 2005.
Decho, A. W.: Microbial biofilms in intertidal systems: an overview, Cont. Shelf Res., 20, 1257–1273, 2000.
delGiorgio, P. A. and France, R. L.: Ecosystem-specific patterns in the relationship between zooplankton and POM or microplankton delta C-13, Limnol. Oceanogr., 41, 359–365, 1996.
Dijkman, N. A. and Kromkamp, J. C.: Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition, Mar. Ecol. -Prog. Ser., 324, 113–125, 2006.
Eilers, P. H. C. and Peeters, J. C. H.: A model for the relationship between light-intensity and the rate of photosynthesis in phytoplankton, Ecolog. Model., 42, 199–215, 1988.
France, R. L.: Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes, Limnol. Oceanogr., 40, 1310–1313, 1995a.
France, R. L.: C-13 enrichment in benthic compared to planktonic algae – foodweb implications, Mar. Ecol.-Prog. Ser., 124, 307–312, 1995b.
France, R. L.: Stable isotopic survey of the role of macrophytes in the carbon flow of aquatic foodwebs, Vegetatio, 124, 67–72, 1996.
Freeman, K. H. and Hayes, J. M.: Fractionation of carbon isotopes by phytoplankton and estimates of ancient CO<sub>2</sub> levels, Global Biogeochem. Cy., 6, 185–198, 1992.
Fry, B. and Wainright, S. C.: Diatom sources of C-13-rich carbon in marine food webs, Mar. Ecol.-Prog. Ser., 76, 149–157, 1991.
Glud, R. N., Ramsing, N. B., and Revsbech, N. P.: Photosynthesis and photosynthesis-coupled respiration in natural biofilms quantified with oxygen microsensors, J. Phycol., 28, 51–60, 1992.
Goericke, R., Montoya, J. P., and Fry, B.: Physiology of isotopic fractionation in algae and cyanobacteria, in: Stable isotopes in ecology and environmental science, edited by: Lajtha, K. and Michner, R. H., Oxford, Blackwell Scientific Publications, 187–221, 1994.
Havens, K. E., East, T. L., Meeker, R. H., Davis, W. P., and Steinman, A. D.: Phytoplankton and periphyton responses to in situ experimental nutrient enrichment in a shallow subtropical lake, J. Plankton Res., 18, 551–566, 1996.
Hayes, J. M.: Factors controlling C-13 contents of sedimentary organic-compounds – Principles and evidence, Mar. Geol., 113, 111–125, 1993.
Johnston, N. T., MacIsaac, E. A., Tschaplinski, P. J., and Hall, K. J.: Effects of the abundance of spawning sockeye salmon (Oncorhynchus nerka) on nutrients and algal biomass in forested streams, Can. J. Fish. Aquat. Sci., 61, 384–403, 2004.
Larned, S. T., Nikora, V. I., and Biggs, B. J. F.: Mass-transfer-limited nitrogen and phosphorus uptake by stream periphyton: A conceptual model and experimental evidence, Limnnol. Oceanogr., 49, 1992–2000, 2004.
Laws, E. A., Popp, B. N., Bidigare, R. R., Kennicutt, M. C., and Macko, S. A.: Dependence of phytoplankton carbon isotopic composition on growth-rate and [CO<sub>2</sub>]$_\rm (Aq)$ – theoretical considerations and experimental results, Geochim. Cosmochim. Ac., 59, 1131–1138, 1995.
Lewis, M. A., Weber, D. E., Goodman, L. R., Stanley, R. S., Craven, W. G., Patrick, J. M., Quarles, R. L., Roush, T. H., and Macauley, J. M.: Periphyton and sediment bioassessment in north Florida Bay, Environ. Monit. Assess., 65, 503–522, 2000.
March, J. G. and Pringle, C. M.: Food web structure and basal resource utilization along a tropical island stream continuum, Puerto Rico, Biotropica, 35, 84–93, 2003.
Rau, G. H., Riebesell, U., and Wolf-Gladrow, D.: A model of photosynthetic C-13 fractionation by marine phytoplankton based on diffusive molecular CO<sub>2</sub> uptake, Mar. Ecol-Pog. Ser., 133, 275–285, 1996.
Roeske, C. and O'Leary, M.: Carbon isotope effect on carboxylation of ribulase biphosphate catalyzed by ribulase biphosphate carboxylase from Rhodospirillum rubrum, Biochemistry, 24, 1603–1607, 1985.
Rost, B., Zondervan, I., and Riebesell, U.: Light-dependent carbon isotope fractionation in the coccolithophorid Emiliania huxleyi, Limnol. Oceanogr., 47, 120–128, 2002.
Schindler, D. E., Carpenter, S. R., Cole, J. J., Kitchell, J. F., and Pace, M. L.: Influence of food web structure on carbon exchange between lakes and the atmosphere, Science, 277, 248–251,1997.
Sidorkewicj, N. S., Lopez Cazorla, A. C., Fernandez, O. A., Mockel, G. C., and Burgos, M. A.: Effects of Cyprinus carpio on Potamogeton pectinatus in experimental culture: the incidence of the periphyton, Hydrobiologia, 415, 13–19, 1999.
Stumm, W. and Morgan, J. J.: Aquatic chemistry: Chemical equilibria and rates in natural waters, New York, Wiley-Interscience, 1995.
Swansburg, E. O., Fairchild, W. L., Fryer, B. J., and Ciborowski, J. J. H.: Mouthpart deformities and community composition of chironomidae (diptera) larvae downstream of metal mines in New Brunswick, Canada. Environ. Toxicol. Chem., 21, 2675–2684, 2002.
Tortell, P. D. and Morel, F. M. M.: Sources of inorganic carbon for phytoplankton in the eastern Subtropical and Equatorial Pacific Ocean, Limnnol. Oceanogr., 47, 1012–1022, 2002.
Trudeau, V. and Rasmussen, J. B.: The effect of water velocity on stable carbon and nitrogen isotope signatures of periphyton, Limnol. Oceanogr., 48, 2194–2199, 2003.
Werne, J. P. and Hollander, D. J.:Balancing supply and demand: controls on carbon isotope fractionation in the Cariaco Basin (Venezuela) Younger Dryas to present, Mar. Chem., 92, 275–293, 2004.
Wolf, G., Picioreanu, C., and van Loosdrecht, M. C. M.: Kinetic modeling of phototrophic biofilms: The PHOBIA model, Biotechnol. Bioeng., 97, 1064–1079, 2007.
Zippel, B. and Neu, T. R.: Growth and structure of phototrophic biofilms under controlled light conditions, Water Sci. Technol., 52, 203–209, 2005.
Zippel, B., Rijstenbil J., and Neu T. R.: A flow-lane incubator for studying freshwater and marine phototrophic biofilms, J. Microbiol. Meth., 70, 336–345, doi:10.1016/j.mimet.2007.05.013, 2007.