Stable carbon isotope discrimination and microbiology of methane formation in tropical anoxic lake sediments

Biogeosciences

Volumn 8, Issue 3, 2011, Pages 795-814

  Conrad, R ^a   Noll, M ^b   Claus, P ^a   Klose, M ^a   Bastos, W R ^c   Enrich Prast, A ^d  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^c University of Rondonia   (Brazil)

^d FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANOXIC CONDITIONS; BIODEGRADATION; CANONICAL ANALYSIS; CARBON DIOXIDE; CARBON ISOTOPE; COMMUNITY COMPOSITION; DISCRIMINANT ANALYSIS; ENZYME ACTIVITY; EXPERIMENTAL STUDY; GENETIC ANALYSIS; INHIBITOR; ISOTOPIC FRACTIONATION; LACUSTRINE DEPOSIT; METHANE; METHANOGENESIS; MICROBIAL COMMUNITY; ORGANIC MATTER; SEDIMENT ANALYSIS; SEDIMENT CHEMISTRY; SPECIES DIVERSITY; STABLE ISOTOPE; TROPICAL ENVIRONMENT;

AMAZONAS [BRAZIL]; BRAZIL;

ARCHAEA; BACTERIA (MICROORGANISMS);

EID: 79953225906     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-8-795-2011     Document Type: Article

References (80)

1. Alperin, M. J., Blair, N. E., Albert, D. B., Hoehler, T. M., and Martens, C. S.: Factors that control the stable carbon isotopic composition of methane produced in an anoxic marine sediment, Global Biogeochem. Cy., 6, 271-291, 1992. (Pubitemid 23376991)
2. Amann, R. I., Ludwig, W., and Schleifer, K. H.: Phylogenetic identification and in situ detection of individual microbial cells without cultivation, Microbiol. Rev., 59, 143-169, 1995.
3. 13C values of pore water methane in a Michigan peatland, Global Biogeochem. Cy., 13, 475-484, 1999.
4. Bastviken, D., Cole, J., Pace, M., and Tranvik, L.: Methane emissions from lakes: Dependence of lake characteristics, two regional assessments, and a global estimate, Global Biogeochem. Cy., 18, GB4009, doi:10.1029/2004GB002238, 2004. (Pubitemid 40440571)
5. Bastviken, D., Santoro, A. L., Marotta, H., Pinho, L. Q., Cal-heiros, D. F., Crill, P., and Enrich-Prast, A.: Methane emission from Pantanal, South America, during low water season: toward more comprehensive sampling, Environ. Sci. Technol., 44, 5450-5455, 2010.
6. Bastviken, D., Tranvik, L. J., Downing, J. A., Crill, P. M., and Enrich-Prast, A.: Freshwater methane emissions offset the continental carbon sink, Science, 331, 50, doi:10.1126/science.1196808, 2011.
7. Bent, S. J. and Forney, L. J.: The tragedy of the uncommon: understanding limitations in the analysis of microbial diversity (Review), ISME J. 2, 689-695, 2008. (Pubitemid 351951570)
8. Billen, G.: Modelling the processes of organic matter degradation and nutrients recycling in sedimentary systems, in: Sediment Microbiology, edited by: Nedwell, D. B. and Brown, C. M., 15-52, Academic Press, 1982.
9. Blair, N., Leu, A., Munoz, E., Olsen, J., Kwong, E., and Des-Marais, D.: Carbon isotopic fractionation in heterotrophic mi-crobial metabolism, Appl. Environ. Microbiol., 50, 996-1001, 1985. (Pubitemid 16228341)
10. Chan, O. C., Claus, P., Casper, P., Ulrich, A., Lueders, T., and Conrad, R.: Vertical distribution of structure and function of the methanogenic archaeal community in Lake Dagow sediment, Environ. Microbiol., 7, 1139-1149, 2005. (Pubitemid 41026514)
11. Cicerone, R. J. and Oremland, R. S.: Biogeochemical aspects of atmospheric methane, Global Biogeochem. Cy., 2, 299-327, 1988. (Pubitemid 19082403)
12. Conrad, R.: Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments (review), FEMS Microbiol. Ecol., 28, 193-202, 1999. (Pubitemid 29123835)
13. Conrad, R.: Quantification of methanogenic pathways using stable carbon isotopic signatures: a review and a proposal, Org. Geochem., 36, 739-752, 2005. (Pubitemid 40561003)
14. Conrad, R.: Soil microbial communities and global climate change - methanotrophic and methanogenic communities as paradigms, in: Modern Soil Microbiology: Second Edition, edited by: VanElsas, J. D., Jansson, J., and Trevors, J. T., 263-282, CRC Press, 2007.
15. Conrad, R. and Klose, M.: How specific is the inhibition by methyl fluoride of acetoclastic methanogenesis in anoxic rice field soil?, FEMS Microbiol. Ecol., 30, 47-56, 1999. (Pubitemid 29393014)
16. 13C-isotopic signature in anoxic rice field soil, Biogeochem., 73, 381-393, 2005. (Pubitemid 40747885)
17. Conrad, R. and Klose, M.: Dynamics of the methanogenic archaeal community in anoxic rice soil upon addition of straw, Eur. J. Soil Sci., 57, 476-484, 2006. (Pubitemid 43965916)
18. Conrad, R. and Klose, M.: Stable carbon isotope discrimination in rice field soil during acetate turnover by syntrophic acetate oxidation or acetoclastic methanogenesis, Geochim. Cosmochim. Ac., 75, 1531-1539, 2011.
19. Conrad, R., Chan, O. C., Claus, P., and Casper, P.: Characterization of methanogenic Archaea and stable isotope fractionation during methane production in the profundal sediment of an oligotrophic lake (Lake Stechlin, Germany), Limnol. Oceanogr., 52, 1393-1406, 2007. (Pubitemid 47121553)
20. Conrad, R., Klose, M., Noll, M., Kemnitz, D., and Bodelier, P. L. E.: Soil type links microbial colonization of rice roots to methane emission, Global Change Biol., 14, 657-669, 2008. (Pubitemid 351228535)
21. Conrad, R., Claus, P., and Casper, P.: Characterization of stable isotope fractionation during methane production in the sediment of a eutrophic lake, Lake Dagow, Germany, Limnol. Oceanogr., 54, 457-471, 2009.
22. Conrad, R., Claus, P., and Casper, P.: Stable isotope fractionation during the methanogenic degradation of organic matter in the sediment of an acidic bog lake, Lake Grosse Fuchskuhle, Lim-nol. Oceanogr., 55, 1932-1942, 2010a.
23. 13C isotope fractionation, and archaeal community composition in the sediment of two clearwater lakes of Amazonia, Limnol. Oceanogr., 55, 689-702, 2010b.
24. DeGraaf, W., Wellsbury, P., Parkes, R. J., and Cappenberg, T. E.: Comparison of acetate turnover in methanogenic and sulfate-reducing sediments by radiolabeling and stable isotope labeling and by use of specific inhibitors: Evidence for isotopic exchange, Appl. Environ. Microbiol., 62, 772-777, 1996. (Pubitemid 26071445)
25. Devol, A. H., Richey, J. E., Forsberg, B. R., and Martinelli, L. A.: Seasonal dynamics in methane emissions from the Amazon River floodplain to the troposphere, J. Geophys. Res., 95, 16417-16426, 1990.
26. Dolfing, J.: Acetogenesis, in: Biology of Anaerobic Microorganisms, eduted by: Zehnder, A. J. B., 417-468, Wiley, 1988.
27. Drake, H. L. and Küsel, K.: How the diverse physiologic potentials of acetogens determine their in situ realities (review), in: Biochemistry and Physiology of Anaerobic Bacteria, edited by: Ljungdahl, L. G., Adams, M. W., Barton, L. L., Ferry, J. G., and Johnson, M. K., 171-190, Springer, 2003.
28. Galand, P. E., Yrjälä, K., and Conrad, R.: Stable carbon isotope fractionation during methanogenesis in three boreal peatland ecosystems, Biogeosciences, 7, 3893-3900, doi:10.5194/bg-7-3893-2010, 2010.
29. Gelwicks, J. T., Risatti, J. B., and Hayes, J. M.: Carbon isotope effects associated with autotrophic acetogenesis, Org. Geochem., 14, 441-446, 1989.
30. Gelwicks, J. T., Risatti, J. B., and Hayes, J. M.: Carbon isotope effects associated with aceticlastic methanogenesis, Appl. Environ. Microbiol., 60, 467-472, 1994. (Pubitemid 24045183)
31. Goevert, D. and Conrad, R.: Effect of substrate concentration on carbon isotope fractionation during acetoclastic methanogenesis by Methanosarcina barkeri and M. acetivorans and in rice field soil, Appl. Environ. Microbiol., 75, 2605-2612, 2009.
32. 13C contents of sedimentary organic compounds: principles and evidence, Mar. Geol., 113, 111-125, 1993. (Pubitemid 24393435)
33. Heitmann, T., Goldhammer, T., Beer, J., and Blodau, C.: Electron transfer of dissolved organic matter and its potential significance for anaerobic respiration in a northern bog, Global Change Biol., 13, 1771-1785, 2007. (Pubitemid 47226274)
34. Heuer, V. B., Krüger, M., Elvert, M., and Hinrichs, K. U.: Experimental studies on the stable carbon isotope biogeochemistry of acetate in lake sediments, Org. Geochem., 41, 22-30, 2010.
35. Hornibrook, E. R. C., Longstaffe, F. J., and Fyfe, W. S.: Evolution of stable carbon isotope compositions for methane and carbon dioxide in freshwater wetlands and other anaerobic environments, Geochim. Cosmochim. Ac., 64, 1013-1027, 2000. (Pubitemid 30231992)
36. Janssen, P. H. and Frenzel, P.: Inhibition of methanogenesis by methyl fluoride - studies of pure and defined mixed cultures of anaerobic bacteria and archaea, Appl. Environ. Microbiol., 63, 4552-4557, 1997. (Pubitemid 27485788)
37. Keller, J. K., Weisenhorn, P. B., and Megonigal, J. P.: Humic acids as electron acceptors in wetland decomposition, Soil Biol. Biochem., 41, 1518-1522, 2009.
38. Klappenbach, J. A., Saxman, P. R., Cole, J. R., and Schmidt, T. M.: rrndb: the ribosomal RNA Operon Copy Number Database, Nucleic Acids Res., 29, 181-184, 2001. (Pubitemid 32054441)
39. Koizumi, Y., Takii, S., Nishino, M., and Nakajima, T.: Vertical distributions of sulfate-reducing bacteria and methane-producing ar-chaea quantified by oligonucleotide probe hybridization in the profundal sediment of a mesotrophic lake, FEMS Microbiol. Ecol., 44, 101-108, 2003. (Pubitemid 37034604)
40. Kolb, S., Knief, C., Dunfield, P. F., and Conrad, R.: Abundance and activity of uncultured methanotrophic bacteria involved in the consumption of atmospheric methane in two forest soils, Environ. Microbiol., 7, 1150-1161, 2005. (Pubitemid 41026515)
41. Krzycki, J. A., Kenealy, W. R., DeNiro, M. J., and Zeikus, J. G.: Stable carbon isotope fractionation by Methanosarcina bark-eri during methanogenesis from acetate, methanol, or carbon dioxide-hydrogen, Appl. Environ. Microbiol., 53, 2597-2599, 1987.
42. Lelieveld, J., Crutzen, P. J., and Dentener, F. J.: Changing concentrations, lifetime and climate forcing of atmospheric methane, Tellus, 50B, 128-150, 1998.
43. Lever, M. A., Alperin, M. J., Teske, A., Heuer, V. B., Schmidt, F., Hinrichs, K. U., Morono, Y., Masui, N., and Inagaki, F.: Aceto-genesis in deep subseafloor sediments of the Juan de Fuca Ridge flank: a synthesis of geochemical, thermodynamic, and gene-based evidence, Geomicrobiol. J., 27, 183-211, 2010.
44. Lovley, D. R. and Klug, M. J.: Methanogenesis from methanol and methylamines and acetogenesis from hydrogen and carbon dioxide in sediments of a eutrophic lake, Appl. Environ. Microbiol., 45, 1310-1315, 1983. (Pubitemid 13132962)
45. Lueders, T., Chin, K. J., Conrad, R., and Friedrich, M.: Molecular analyses of methyl-coenzyme M reductase alpha-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage, Environ. Microbiol., 3, 194-204, 2001. (Pubitemid 33136743)
46. Marani, L. and Alvala, P. C.: Methane emissions from lakes and floodplains in Pantanal, Brazil, Atmos. Environ., 41, 1627-1633, 2007. (Pubitemid 46151793)
47. McInerney, M. J. and Bryant, M. P.: Basic principles of bioconver-sions in anaerobic digestion and methanogenesis, in: Biomass Conversion Processes for Energy and Fuels, edited by: Sofer, S. S. and Zaborsky, O. R., 277-296, Plenum, 1981.
48. Noll, M., Klose, M., and Conrad, R.: Effect of temperature change on the composition of the bacterial and archaeal community potentially involved in the turnover of acetate and propionate in methanogenic rice field soil, FEMS Microbiol. Ecol., 73, 215-225, 2010.
49. Nüsslein, B., Chin, K. J., Eckert, W., and Conrad, R.: Evidence for anaerobic syntrophic acetate oxidation during methane production in the profundal sediment of subtropical Lake Kinneret (Israel), Environ. Microbiol., 3, 460-470, 2001. (Pubitemid 33136730)
50. Nüsslein, B., Eckert, W., and Conrad, R.: Stable isotope biogeo-chemistry of methane formation in profundal sediments of Lake Kinneret (Israel), Limnol. Oceanogr., 48, 1439-1446, 2003. (Pubitemid 36964764)
51. Pace, N. R.: A molecular view of microbial diversity and the biosphere, Science, 276, 734-740, 1997. (Pubitemid 27199842)
52. Penning, H. and Conrad, R.: Carbon isotope effects associated with mixed-acid fermentation of saccharides by Clostridium papyro-solvens, Geochim. Cosmochim. Ac., 70, 2283-2297, 2006.
53. Penning, H., Plugge, C. M., Galand, P. E., and Conrad, R.: Variation of carbon isotope fractionation in hydrogenotrophic methanogenic microbial cultures and environmental samples at different energy status, Global Change Biol., 11, 2103-2113, 2005. (Pubitemid 43904648)
54. Penning, H., Claus, P., Casper, P., and Conrad, R.: Carbon isotope fractionation during acetoclastic methanogenesis by Methanosaeta concilii in culture and a lake sediment, Appl. Environ. Microbiol., 72, 5648-5652, 2006.
55. Quay, P. D., King, S. L., Stutsman, J., Wilbur, D. O., Steele, L. P., Fung, I., Gammon, R. H., Brown, T. A., Farwell, G. W., Grootes, P. M., and Schmidt, F. H.: Carbon isotopic composition of atmospheric CH4: fossil and biomass burning source strengths, Global Biogeochem. Cy., 5, 25-47, 1991.
56. Rappe, M. S. and Giovannoni, S. J.: The uncultured microbial majority, Ann. Rev. Microbiol., 57, 369-394, 2003. (Pubitemid 37392948)
57. Rinaldi, G., Meinschein, W. G., and Hayes, J. M.: Carbon isotope fractionations associated with acetic acid production by Aceto-bacter suboxydans, Biomed. Mass Spectrometry, 1, 412-414, 1974.
58. Rothfuss, F. and Conrad, R.: Thermodynamics of methanogenic intermediary metabolism in littoral sediment of Lake Constance, FEMS Microbiol. Ecol., 12, 265-276, 1993.
59. Schink, B. and Zeikus, J. G.: Microbial ecology of pectin decomposition in anoxic lake sediments, J. Gen. Microbiol., 128, 393-404, 1982.
60. Schink, B. and Stams, A. J. M.: Syntrophism among prokaryotes, in: The Prokaryotes, Edn. 3, Vol. 2, edited by: Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. H., and Stackebrandt, E., 309-335, Springer, 2006.
61. Schwarz, J. I. K., Eckert, W., and Conrad, R.: Community structure of Archaea and Bacteria in a profundal lake sediment Lake Kinneret (Israel), Syst. Appl. Microbiol., 30, 239-254, 2007a. (Pubitemid 46428502)
62. Schwarz, J. I. K., Lueders, T., Eckert, W., and Conrad, R.: Identification of acetate-utilizing Bacteria and Archaea in methanogenic profundal sediments of Lake Kinneret (Israel) by stable isotope probing of rRNA, Environ. Microbiol., 9, 223-237, 2007b. (Pubitemid 46059013)
63. Smith, L. K., Lewis, W. M., Chanton, J. P., Cronin, G., and Hamilton, S. K.: Methane emissions from the Orinoco River flood-plain, Venezuela, Biogeochem., 51, 113-140, 2000.
64. Stumm, W. and Morgan, J. J.: Aquatic Chemistry, An Introduction Emphasizing Chemical Equilibria in Natural Waters, Wiley, 1981.
65. 2, Geochim. Cosmochim. Ac., 57, 4015-4027, 1993. (Pubitemid 24395622)
66. 4 production by a hyperthermophilic methanogen under high-pressure cultivation, Proc. Natl. Acad. Sci. USA, 105, 10949-10954, 2008.
67. Tijhuis, L., VanLoosdrecht, M. C. M., and Heijnen, J. J.: A ther-modynamically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth, Biotechnol. Bioeng., 42, 509-519, 1993. (Pubitemid 23211031)
68. 4 + OH, edited by: Kaye, J. A., 390-408, American Chemical Society, 1992.
69. Valentine, D. L., Chidthaisong, A., Rice, A., Reeburgh, W. S., and Tyler, S. C.: Carbon and hydrogen isotope fractionation by moderately thermophilic methanogens, Geochim. Cosmochim. Ac., 68, 1571-1590, 2004. (Pubitemid 38464301)
70. Ward, D. M. and Winfrey, M. R.: Interactions between methanogenic and sulfate-reducing bacteria in sediments, Adv. Aquat. Microbiol., 3, 141-179, 1985.
71. Wassmann, R., Thein, U. G., Whiticar, M. J., Rennenberg, H., Seiler, W., and Junk, W. J.: Methane emissions from the Amazon floodplain: characterization of production and transport, Global Biogeochem. Cy., 6, 3-13, 1992.
72. Whiticar, M. J.: Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane, Chem. Geology, 161, 291-314, 1999. (Pubitemid 30130536)
73. 2 reduction vs. acetate fermentation - isotopic evidence, Geochim. Cos-mochim. Ac., 50, 693-709, 1986.
74. Woese, C. R.: Interpreting the universal phylogenetic tree, Proc. Natl. Acad. Sci. USA, 97, 8392-8396, 2000. (Pubitemid 30639683)
75. Yavitt, J. B. and Seidmann-Zager, M.: Methanogenic conditions in northern peat soils, Geomicrobiol. J., 23, 119-127, 2006. (Pubitemid 43347968)
76. Zehnder, A. J. B.: Ecology of methane formation, in: Water Pollution Microbiology, edited by: Mitchell, R., Vol. 2., 349-376, Wiley, 1978.
77. Zepp-Falz, K., Holliger, C., Grosskopf, R., Liesack, W., Nozhevnikova, A. N., Müller, B., Wehrli, B., and Hahn, D.: Vertical distribution of methanogens in the anoxic sediment of Rot-see (Switzerland), Appl. Environ. Microbiol., 65, 2402-2408, 1999.
78. Zhang, C. L. L., Ye, Q., Reysenbach, A. L., Gotz, D., Peacock, A., White, D. C., Horita, J., Cole, D. R., Fong, J., Pratt, L., Fang, J. S., and Huang, Y. S.: Carbon isotopic fractionations associated with thermophilic bacteria Thermotoga maritima and Perse-phonella marina, Environ. Microbiol., 4, 58-64, 2002. (Pubitemid 34276123)
79. Zhang, G. S., Jiang, N., Liu, X. L., and Dong, X. Z.: Methanogen-esis from methanol at low temperatures by a novel psychrophilic methanogen, "Methanolobus psychrophilus" sp nov., prevalent in Zoige wetland of the Tibetan plateau, Appl. Environ. Microbiol., 74, 6114-6120, 2008.
80. Zinder, S. H.: Physiological ecology of methanogens, in: Methano-genesis. Ecology, Physiology, Biochemistry and Genetics, edited by: Ferry, J. G., 128-206, Chapman & Hall, 1993.