[en] We quantified chemoautotrophic and anoxygenic photosynthetic microbial production in the water column of Lake Kivu, a permanently stratified tropical lake situated amidst volcanic activity, and aimed to identify the microorganisms involved in these processes through the analysis of their phospholipid fatty acid (PLFA) content and stable isotope (13C) labelling of PLFA in a set of incubation experiments. Data demonstrate the existence of a biogeochemically active chemoautotrophic bacterial community in the redoxcline of Lake Kivu (50–70 m). PLFA data indicate that the bacterial communities are structured vertically in the water column, with a large dissimilarity between the oxic and anoxic waters. Maximum volumetric dark CO2 fixation rates measured in Lake Kivu were in the same range as values reported from H2S-rich marine redoxclines, such as the Black and Baltic Seas, and the Cariaco Basin. Similarly, maximal chemoautotrophic activities in Lake Kivu were observed in sulfidic waters, just below the oxycline. Anoxygenic photosynthetic production was never observed in the main basin of Lake Kivu. However, anoxygenic phototrophs largely dominated CO2 fixation in the illuminated redoxcline of Kabuno Bay, a shallower ferruginous sub-basin. Overall, this study supports the idea that chemoautotrophs and/or anoxygenic photoautotrophs might play an important role in the flow of carbon and energy in permanently stratified tropical ecosystems. In Lake Kivu, these processes significantly contribute to organic matter biosynthesis and exert an indirect control on oxygenic photoautotrophs by shortcircuiting the vertical transport of nutrients to the illuminated and oxygenated surface waters.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Morana, Cédric ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (COU)
Roland, Fleur ; Université de Liège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)
Crowe, Sean A.
Llirós, Marc
Borges, Alberto ; Université de Liège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)
Darchambeau, François ; Université de Liège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)
Bouillon, Steven
Language :
English
Title :
Chemoautotrophy and anoxygenic photosynthesis within the water column of a large meromictic tropical lake (Lake Kivu, East Africa)
Borges, A. V., G. Abril, B. Delille, J.-P. Descy, and F. Darchambeau. 2011. Diffusive methane emissions to the atmosphere from Lake Kivu (Eastern Africa). J. Geophys. Res. 116: G03032. doi:10.1029/2011JG001673
Boschker, H. T. S. 2004. Linking microbial community structure and functioning: stable istope (13C) labeling in combination with PLFA analysis, p. 1673–1688. In G. A. Kowalchuk, F. J. de Bruijn, I. M. Head, A. D. L. Akkermans, & J. D. van Elsas (Eds.), Molecular Microbial Ecology Manual, 2nd edition. Kluwer Academic Publishers.
Canfield, D. E., M. T. Rosing, and C. Bjerrum. 2006. Early anaerobic metabolisms. Philos. Trans. R. Soc. B Biol. Sci. 361: 1819–1836. doi:10.1098/rstb.2006.1906
Cline, J. D. 1969. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14: 454–458. doi:10.4319/lo.1969.14.3.0454
Cole, J. J., and others. 2007. Plumbing the global carbon cycle: Integrating inland waters into the terrestrial carbon budget. Ecosystems 10: 171–184. doi:10.1007/s10021-006-9013-8
Crowe, S. A., and others. 2008. Photoferrotrophs thrive in an Archean Ocean analogue. Proc. Natl. Acad. Sci. 105: 15938–15943. doi:10.1073/pnas.0805313105
Crowe, S. A., and others. 2014. Deep-water anoxygenic photosythesis in a ferruginous chemocline. Geobiology 12: 322–339. doi:10.1111/gbi.12089
Darchambeau, F., H. Sarmento, and J.-P. Descy. 2014. Primary production in a tropical large lake: The role of phytoplankton composition. Sci. Total Environ. 473: 178–188. doi:10.1016/j.scitotenv.2013.12.036
Enrich-Prast, A., D. Bastviken, and P. M. Crill. 2009. Chemosynthesis, p. 221–225. In G. Likens [ed.], Encyclopedia of inland waters. Springer.
Farías, L., C. Fernández, J. Faúndez, M. Cornejo, and M. E. Alcaman. 2009. Chemolithoautotrophic production mediating the cycling of the greenhouse gases N2O and CH4 in an upwelling ecosystem. Biogeosciences 6: 3053–3069. doi:10.5194/bg-6-3053-2009
García-Cantizano, J., E. O. Casamayor, J. M. Gasol, R. Guerrero, and C. Pedrós-Alió. 2005. Partitioning of CO2 incorporation among planktonic microbial guilds and estimation of in situ specific growth rates. Microb. Ecol. 50: 230–241. doi:10.1007/s00248-004-0144-9
Gillikin, D. P., and S. Bouillon. 2007. Determination of δ18O of water and δ13C of dissolved inorganic carbon using a simple modification of an elemental analyser-isotope ratio mass spectrometer: An evaluation. Rapid Commun. Mass Spectrom. 21: 1475–1478. doi:10.1002/rcm.2968
Glaubitz, S., T. Lueders, W. R. Abraham, G. Jost, K. Jürgens, and M. Labrenz. 2009. 13C-isotope analyses reveal that chemolithoautotrophic Gamma-and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea. Environ. Microbiol. 11: 326–337. doi:10.1111/j.1462-2920.2008.01770.x
Grogan, D. W., and J. E. Cronan. 1997. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61: 429–441.
Grote, J., G. Jost, M. Labrenz, G. J. Herndl, and K. Jürgens. 2008. Epsilonproteobacteria represent the major portion of chemoautotrophic bacteria in sulfidic waters of pelagic redoxclines of the Baltic and Black Seas. Appl. Environ. Microbiol. 74: 7546–7551. doi:10.1128/AEM.01186-08
Haberyan, K. A., and R. E. Hecky. 1987. The late Pleistocene and Holocene stratigraphy and paleolimnology of Lakes Kivu and Tanganyika. Palaeogeogr. Palaeoclimatol. Palaeoecol. 61: 169–197. doi:10.1016/0031-0182(87)90048-4
Hadas, O., R. Pinkas, and J. Erez. 2001. High chemoautotrophic primary production in Lake Kinneret, Israel: A neglected link in the carbon cycle of the lake. Limnol. Oceanogr. 46: 1968–1976. doi:10.4319/lo.2001.46.8.1968
Heising, S., L. Richter, W. Ludwig, and B. Schink. 1999. Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain. Arch. Microbiol. 172: 116–124. doi:10.1007/s002030050748
Imhoff, J. F. 2003. Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna–Matthews–Olson protein) gene sequences. Int. J. Syst. Evol. Microbiol. 53: 941–951. doi:10.1099/ijs.0.02403-0
İnceoğlu, O., and others. 2015a. Distribution of bacteria and archea in meromictic tropical Lake Kivu. Aquat. Microb. Ecol. 74: 215–233. doi:10.3354/ame01737
İnceoğlu, O., and others. 2015b. Vertical distribution of functional potential and active microbial communities in meromictic Lake Kivu. Microb. Ecol. 70: 596–611. doi:10.1007/s00248-015-0612-9
Jørgensen, B. B., J. G. Kuenen, and Y. Cohen. 1979. Microbial transformations of sulfur compounds in a stratified lake (Solar Lake, Sinai). Limnol. Oceanogr. 24: 799–822. doi:10.4319/lo.1979.24.5.0799
Jørgensen, B. B., H. Fossing, C. O. Wirsen, and H. W. Jannasch. 1991. Sulfide oxidation in the anoxic Black Sea chemocline. Deep-Sea Res. Part A Oceanogr. Res. Pap. 38: S1083–S1103. doi:10.1016/S0198-0149(10)80025-1
Jost, G., M. V. Zubkov, E. Yakushev, M. Labrenz, and K. Jurgens. 2008. High abundance and dark CO2 fixation of chemolithoautotrophic prokaryotes in anoxic waters of the Baltic Sea. Limnol. Oceanogr. 53: 14–22. doi:10.4319/lo.2008.53.1.0014
Kelly, D. P. 1990. Energetics of chemolithotrophs, p. 479–503. In T. A. Krulwich [ed.], Bacterial energetics. Academic Press.
Kilham, P., and S. S. Kilham. 1990. Endless summer: Internal loading processes dominate nutrient cycling in tropical lakes. Freshw. Biol. 23: 379–389. doi:10.1111/j.1365-2427.1990.tb00280.x
Le Bodelier, P., M.-J. Bär Gillisen, K. Hordijk, J. S. Sinninghe Damsté, I. C. Rijpstra, J. A. J. Geenevasen, and P. F. Dunfield. 2009. A reanalysis of phospholipid fatty acids as ecological biomarkers for methanotrophic bacteria. ISME J. 3: 606–617. doi:10.1038/ismej.2009.6
Li, Y. L., A. D. Peacock, D. C. White, R. Geyer, and C. L. Zhang. 2007. Spatial patterns of bacterial signature biomarkers in marine sediments of the Gulf of Mexico. Chem. Geol. 238: 168–179. doi:10.1016/j.chemgeo.2006.11.007
Li, X. N., G. T. Taylor, Y. Astor, R. Varela, and M. I. Scranton. 2012. The conundrum between chemoautotrophic production and reductant and oxidant supply: A case study from the Cariaco Basin. Deep-Sea Res. Part I Oceanogr. Res. Pap. 61: 1–10. doi:10.1016/j.dsr.2011.11.001
Llirós, M., and others. 2010. Vertical distribution of ammonia-oxidizing crenarchaeota and methanogens in the epipelagic waters of Lake Kivu (Rwanda – Democratic Republic of the Congo). Appl. Environ. Microbiol. 76: 6853–6863. doi:10.1128/AEM.02864-09
Llirós, M., and others. 2015. Pelagic photoferrotrophy and iron cycling in a modern ferruginous basin. Scientific Reports, 5, 13803. doi:10.1038/srep13803
Marschall, E., M. Jogler, U. Henssge, and J. Overmann. 2010. Large-scale distribution and activity patterns of an extremely low-light adapted population of green sulphur bacteria in the Black Sea. Environ. Microbiol. 12: 1348–1362. doi:10.1111/j.1462-2920.2010.02178.x
Middelburg, J. J. 2011. Chemoautotrophy in the ocean. Geophys. Res. Lett. 38. doi:10.1029/2011GL049725
Mizoguchi, T., Y. Tsukatani, J. Harada, S. Takasaki, T. Yoshitomi, and H. Tamiaki. 2013. Cyclopropane-ring formation in the acyl groups of chlorosome glycolipids is crucial for acid resistance of green bacterial antenna systems. Bioorg. Med. Chem. 21: 3689–3694. doi:10.1016/j.bmc.2013.04.030
Morana, C., A. V. Borges, F. A. E. Roland, F. Darchambeau, J.-P. Descy, and S. Bouillon. 2015. Methanotrophy within the water column of a large meromictic tropical lake (Lake Kivu, East Africa). Biogeosciences 12: 2077–2088. doi:10.5194/bg-12-2077-2015
Murray, J. W., L. A. Codispoti, and G. E. Friederich. 1995. Oxidation-reduction environments: The suboxic zone in the Black Sea, p. 157–176. In C. P. Huang, C. R. O'Melia and J. J. Morgan [eds.], Aquatic chemistry: Interfacial and interspecies processes. American Chemical Society: Advances in Chemistry Series, v. 244.
Noguerola, I., A. Picazo, M. Llirós, A. Camacho, and C. M. Borrego. 2015. Diversity of freshwater Epsilonproteobacteria and dark inorganic carbon fixation in the sulphidic redoxcline of a meromictic karstic lake. FEMS Microbiol. Ecol. 91: fiv086. doi: 10.1093/femsec/fiv086
Overmann, J., H. Cypionka, and N. Pfennig. 1992. An extremely low-light-adapted phototrophic sulfur bacterium from the Black Sea. Limnol. Oceanogr. 37: 150–155. doi:10.4319/lo.1992.37.1.0150
Overmann, J., T. Beatty, and K. J. Hall. 1996. Purple sulfur bacterial control the growth of aerobic heterotrophic bacterioplankton in a meromictic salt lake. Appl. Environ. Microbiol. 62: 3251–3258.
Pasche, N., C. Dinkel, B. Müller, M. Schmid, A. Wüest, and B. Wehrli. 2009. Physical and bio-geochemical limits to internal nutrient loading of meromictic Lake Kivu. Limnol. Oceanogr. 54: 1863–1873. doi:10.4319/lo.2009.54.6.1863
Schmid, M., M. Halbwachs, B. Wehrli, and A. Wüest. 2005. Weak mixing in Lake Kivu: New insights indicate increasing risk of uncontrolled gas eruption. Geochem. Geophys. Geosyst. 6: Q07009. doi:10.1029/2004GC000892
Sirevåg, R., B. B. Buchanan, J. A. Berry, and J. H. Troughton. 1977. Mechanisms of CO2 fixation in bacterial photosynthesis studied by the carbon isotope fractionation technique. Arch. Microbiol. 112: 35–38. doi:10.1007/BF00446651
Taipale, S., R. I. Jones, and M. Tiirola. 2009. Vertical diversity of bacteria in an oxygen-stratified lake, evaluated using DNA and phospholipid analyses. Aquat. Microb. Ecol. 55: 1–16. doi:10.3354/ame01277
Taylor, G. T., M. Iabichella, T. Y. Ho, M. I. Scranton, R. C. Thunell, F. Muller-Karger, and R. Varela. 2001. Chemoautotrophy in the redox transition zone of the Cariaco Basin: A significant midwater source of organic carbon production. Limnol. Oceanogr. 46: 150–155. doi:10.4319/lo.2001.46.1.0148
Thiery, W., A. Martynov, F. Darchambeau, J. Descy, P. Plisnier, L. Sushama, and N. Van Lipzig. 2014. Understanding the performance of the FLake model over two African Great Lakes. Geosci. Model Dev. 7: 317–337. doi:10.5194/gmd-7-317-2014
Viollier, E., P. W. Inglett, K. Hunter, A. N. Roychoudhury, and P. Van Cappellen. 2000. The ferrozine method revisited: Fe (II)/Fe (III) determination in natural waters. Appl. Geochem. 15: 785–790. doi:10.1016/S0883-2927(99)00097-9
Weiss, R. F. 1981. Determinations of carbon dioxide and methane by dual catalyst flame ionization chromatography and nitrous oxide by electron capture chromatography. J. Chromatogr. Sci. 19: 611–616. doi:10.1093/chromsci/19.12.611
Wenk, C. B., and others. 2013. Anaerobic ammonium oxidation (anammox) bacteria and sulfide-dependent denitrifiers coexist in the water column of a meromictic south-alpine lake. Limnol. Oceanogr. 58: 1–12. doi:10.4319/lo.2013.58.1.0001
Zhang, Y. M., and C. O. Rock. 2008. Membrane lipid homeostasis in bacteria. Nat. Rev. Microbiol. 6: 222–233. doi:10.1038/nrmicro1839
Zigah, P. K., K. Oswald, A. Brand, C. Dinkel, B. Wehrli, and C. Schubert. 2015. Methane oxidation pathways and associated methanotrophic communities in the water column of a tropical lake. Limnol. Oceanogr. 60: 553–572. doi:10.1002/lno.10035