Abstract
The atmospheric concentration of methane (CH4), a major greenhouse gas, is mainly controlled by the activities of CH4-producing (methanogens) and CH4-consuming (methanotrophs) microorganisms. Freshwater lakes are identified as one of the main CH4 sources, as it is estimated that they contribute to 6–16 % of natural CH4 emissions. It is therefore critical to better understand the biogeochemical cycling of CH4 in these ecosystems.
In this vein, the Lake Pavin provides a useful microbial ecosystem to investigate CH4 cycle in freshwater systems. Despite a significant production of CH4 in the deep anoxic water column and sediment, the amounts of CH4 emitted by Lake Pavin to the atmosphere are several orders of magnitude lower than those of temperate lakes suggesting intense consumption activities of this gas.
This chapter focuses on CH4 cycle, but as methanogenesis and anaerobic methanotrophy build competitive and cooperative relationships with a number of bacterial metabolic groups, we also address bacterial processes that are tightly coupled with CH4 cycle (e.g., ferric iron reduction). Three main sections constitute this chapter:
-
A presentation of CH4 cycle, including methanogenesis and methanotrophy, in freshwater systems and particularly in Lake Pavin,
-
The relationships between CH4 cycle and some other biogeochemical processes in Lake Pavin (ferric iron reduction, sulfate reduction and fermentation), including a brief overview of anaerobic microbial metabolisms,
-
Sections on methodologies enabling to access informations on the anaerobic metabolisms (e.g., biomarkers, isotopes, microcalorimetry, nucleic acid molecular markers, magnetoFISH).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
Abbreviations
- ANME:
-
Anaerobic Methanotrophs
- AOM:
-
Anaerobic Oxidation of Methane
- CARD:
-
Catalyzed Reporter Deposition
- CLSM:
-
Confocal Laser Scanning Microscopy
- DAPI:
-
Diamidino-2-phenylindole
- FISH:
-
Fluorescent in situ hybridization
- FRB:
-
Ferric Iron Reducing Bacteria
- HRP:
-
Horseradish Peroxidase
- MBGD:
-
Marine Benthic Group D
- MMO:
-
Methane Mono-Oxygenase
- MPR:
-
Methane Production Rate
- NRB:
-
Nitrate Reducing Bacteria
- pMMO:
-
Particulate Methane Mono-Oxygenase
- p.p.m.:
-
Parts Per Millions
- PLFA:
-
Phospholipids Fatty Acids
- rRNA:
-
Ribosomal RNA
- sMMO:
-
Soluble Methane Mono-Oxygenase
- SRB:
-
Sulfate Reducing Bacteria
- TEM:
-
Transmission Electron Microscopy
References
Amann R, Fuchs BM (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat Rev Microbiol 6:339–348
Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862
Auguet JC, Barberan A, Casamayor EO (2010) Global ecological patterns in uncultured Archaea. ISME J 4:182–190
Bapteste E, Brochier C, Boucher Y (2005) Higher-level classification of the Archaea: evolution of methanogenesis and methanogens. Archaea 1:353–363
Bastviken D (2009) Methane. In: Likens G (ed) Encyclopedia of inland waters. Elsevier, Oxford, pp 783–805
Bastviken D, Ejlertsson J, Tranvik L (2002) Measurement of methane oxidation in lakes- a comparison of methods. Environ Sci Technol 36:3354–3361
Bastviken D, Ejlertsson J, Sundh I, Tranvik L (2003) Methane as a source of carbon and energy for lake pelagic food webs. Ecology 84:969–981
Bastviken D, Cole J, Pace M, Tranvik L (2004) Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Global Biogeochem Cycles 18:GB4009
Bastviken D, Cole JJ, Pace ML, Van de Bogert MC (2008) Fates of methane from different lake habitats: connecting whole-lake budgets and CH4 emissions. J Geophys Res 113:G02024
Battistuzzi FU, Feijao A, Hedges SB (2004) A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 4:44
Beal EJ, House CH, Orphan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325:184–187
Bedard C, Knowles R (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH4 +, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev 53:68–84
Belaich JP (1980) Growth and metabolism in bacteria. In: Beezer AE (ed) Biological microcalorimetry. Academic, London, pp 1–42
Belova SE, Baani M, Suzina NE, Bodelier PLE, Liesack W, Dedysh SN (2011) Acetate utilization as a survival strategy of peat-inhabiting Methylocystis spp. Environ Microbiol Rep 3:36–46
Biderre-Petit C, Jézéquel D, Dugat-Bony E, Lopes F, Kuever J, Borrel G, Viollier E, Fonty G, Peyret P (2011) Identification of microbial communities involved in the methane cycle in a freshwater meromictic lake. FEMS Microbiol Ecol 77:533–545
Birgel D, Peckmann J (2008) Aerobic methanotrophy at ancient marine methane seeps: a synthesis. Org Geochem 39:1659–1667
Birou B, von Stockar U (1989) Application of bench-scale calorimetry to chemostat cultures. Enzyme Microb Technol 11:12–16
Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jorgensen BB, Witte U et al (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626
Borrel G, Jézéquel D, Biderre-Petit C, Morel-Desrosiers N, Morel JP, Peyret P, Fonty G, Lehours AC (2011) Production and consumption of methane in freshwater lake ecosystems. Res Microbiol 162:832–847
Borrel G, Lehours AC, Crouzet O, Jézéquel D, Rockne D, Kulczak A, Duffaud E, Joblin K, Fonty G (2012a) Stratification of Archaea in the deep sediments of a freshwater meromictic lake: vertical shift from methanogenic to uncultured archaeal lineages. PlosOne 7:e43346
Borrel G, Joblin K, Guedon A, Colombet J, Tardy V, Lehours AC, Fonty G (2012b) Methanobacterium lacus sp. nov., isolated from the profundal sediment of a freshwater meromictic lake. Int J Syst Evol Microbiol 62:1625–1629
Borrel G, Colombet J, Robin A, Lehours AC, Prangishvili D, Sime-Ngando T (2012c) Unexpected and novel putative viruses in the sediments of a deep-dark permanently anoxic freshwater habitat. ISME J 6:2119–2127
Borrel G, O’Toole PW, Harris HM, Peyret P, Brugère JF, Gribaldo S (2013) Phylogenomic data support a seventh order of methylotrophic methanogens and provide insights into the evolution of methanogenesis. Genome Biol Evol 5:1769–1780
Borrel G, Parisot N, Harris HMB, Peyrtaillade E, Gaci N, Tottey W, Bardot O, Raymann K, Gribaldo S, Peyret P, O’Toole PW, Brugère JF (2014) Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 15:679
Braissant O, Bonkat G, Wirz D, Bachmann A (2013) Microbial growth and isothermal microcalorimetry: growth models and their application to microcalorimetric data. Thermochimica Acta 555:64–71
Bricheux G, Bonnet JL, Bohatier J, Morel JP, Morel-Desrosiers N (2013) Microcalorimetry: a powerful and original tool for tracking the toxicity of a xenobiotic on Tetrahymena pyriformis. Ecotoxicol Environ Saf 98:88–94
Briee C, Moreira D, Lopez-Garcia P (2007) Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Res Microbiol 158:213–227
Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252
Brugère JF, Borrel G, Gaci N, Tottey W, O’Toole PW, Malpuech-Brugère C (2013) Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes 5:5–10
Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5:89–96
Case RJ, Boucher Y, Dahllof I, Holmstrom C, Doolittle WF, Kelleberg S (2007) Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl Environ Microbiol 73:278–288
Chan OC, Claus P, Casper P, Ulrich A, Lueders T, Conrad R (2005) Vertical distribution of structure and function of the methanogenic archaeal community in Lake Dagow sediment. Environ Microbiol 7:1139–1149
Cicerone RJ, Oremland RS (1988) Biogeochemical aspects of atmospheric methane. Global Biogeochem Cycles 2:299–327
Conrad R (1999) Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments. FEMS Microbiol Ecol 28:193–202
Conrad R (2009) The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Rep 1:285–292
Conrad R, Klose M, Claus P, Enrich-Prast A (2010) Methanogenic pathway, C-13 isotope fractionation, and archaeal community composition in the sediment of two clear-water lakes of Amazonia. Limnol Oceanogr 55:689–702
Costello AM, Auman AJ, Macalady JL, Scow KM, Lidstrom ME (2002) Estimation of methanotroph abundance in a freshwater lake sediment. Environ Microbiol 4:443–450
Dedysh SN, Knief C, Dunfield PF (2005) Methylocella species are facultatively methanotrophic. J Bacteriol 187:4665–4670
Dedysh SN, Belova SE, Bodelier PLE, Smirnova KV, Khmelenina VN, Chidthaisong A, Trotsenko YA, Liesack W, Dunfield PF (2007) Methylocystis heyeri sp. nov., a novel type II methanotrophic bacterium possessing ‘signature’ fatty acids of type I methanotrophs. Int J Syst Evol Microbiol 57:472–479
Deines P, Grey J, Richnow HH, Eller G (2007) Linking larval chironomids to methane: seasonal variation of the microbial methane cycle and chironomid delta C-13. Aquat Microb Ecol 46:273–282
Drake HL, Daniel SL, Matthies C, Küsel K (1994) Acetogenesis, acetogenic bacteria, and the acethyl-CoA pathway: past and current perspectives. In: Drake HL (ed) Acetogenesis. Chapman and Hall, New York, pp 3–60
Drake HL, Küsel K, Matthies C (2006) Acetogenic prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH (eds) The prokaryotes, vol 2, Ecophysiology and biochemistry. Springer, New York, pp 354–420
Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Mirobiol 62:1902–1907
Dubrunfault M (1856) Note sur la chaleur et le travail mécanique produits par la fermentation vineuse. Compt Rend 42:945–948
Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou SB, Ly B, Saw JH, Zhou ZM, Ren Y, Wang JM, Mountain BW, Crowe MA, Weatherby TM, Bodelier PLE, Liesack W, Feng L, Wang L, Alam M (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450:879–882
Dunfield PF, Belova SE, Vorob’ev AV, Cornish SL, Dedysh SN (2010) Methylocapsa aurea sp. nov., a facultative methanotroph possessing a particulate methane monooxygenase, and emended description of the genus Methylocapsa. Int J Syst Evol Microbiol 60:2659–2664
Ehrlich HL, Newman DK (2008) Geomicrobiology of iron. In: Ehrilich HL, Newman DK (eds) Geomicrobiology, vol 5. CRC Press, Boca Raton, pp 279–329
EPA (United States Environmental Protection Agency) (2010) Methane and nitrous oxide emissions from natural sources. Office of atmospheric programs, Washington. Available at http://www.epa.gov/outreach/pdfs/Methane-and-Nitrous-Oxide-Emissions-From-Natural-Sources.pdf
Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, Op den Camp HJM, Jetten MSM, Strous M (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10:3164–3173
Ettwig KF, van Alen T, van de Pas-Schoonen KT, Jetten MSM, Strous M (2009) Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol 75:3656–3662
Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MMM, Schreiber F, Dutilh BE, Zedelius J et al (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548
Ferry JG (2010) The chemical biology of methanogenesis. Planet Space Sci 58:1775–1783
Frenzel P (2000) Plant-associated methane oxidation in rice fields and wetlands. Adv Microb Ecol 16:85–114
Fricke WF, Seedorf H, Henne A, Kruer M, Liesegang H, Hedderich R, Gottschalk G, Thauer RK (2006) The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. J Bacteriol 188:642–658
Garcia JL (1990) Taxonomy and ecology of methanogens. FEMS Microbiol Rev 87:297–308
Garcia JL, Patel BKC, Ollivier B (2000) Taxonomic, phylogenetic and ecological diversity of methanogenic archaea. Anaerobe 6:205–226
Glissmann K, Chin KJ, Casper P, Conrad R (2004) Methanogenic pathway and archaeal community structure in the sediment of eutrophic Lake Dagow: effect of temperature. Microb Ecol 48:389–399
Grossart HP, Frindte K, Dziallas C, Eckert W, Tang KW (2011) Microbial methane production in oxygenated water column of an oligotrophic lake. Proc Natl Acad Sci U S A 108:19657–19661
Guimbaud C, Catoire V, Gogo S, Robert C, Chartier M, Laggoun-Défarge F, Grossel A, Albéric P, Pomathiod L, Nicoullaud B, Richard G (2011) A portable infrared laser spectrometer for flux measurements of trace gases at the geosphere-atmosphere interface. Meas Sci Technol 22:1–17
Gustafsson L (1991) Microbiological calorimetry. Thermochimica Acta 193:145–171
Hallam SJ, Girguis PR, Preston CM, Richardson PM, DeLong EF (2003) Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea. Appl Environ Microbiol 69:5483–5491
Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, Richardson PM, DeLong EF (2004) Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305:1457–1462
Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471
Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholz P, Yuan Z, Tyson GW (2013) Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500:567–570
Harrison BK, Zhang H, Berelson W, Orphan VJ (2009) Variations in archaeal and bacterial diversity associated with the sulfate-methane transition zone in continental margin sediments (Santa Barbara Basin, California). Appl Environ Microbiol 75:1487–1499
Hedderich R, Whitman W (2006) Physiology and biochemistry of the methane-producing Archaea. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 1050–1079
Ianotti EL, Kafkewitz D, Wolin MJ, Bryant MP (1973) Glucose fermentation products of Ruminococcus albus grown in continuous culture with Vibrio succinogenes: changes caused by interspecies transfer of H2. J Bacteriol 114:1231–1240
Iino T, Tamaki H, Tamazawa S, Ueno Y, Ohkuma M, Suzuki K, Igarashi Y, Haruta S (2013) Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata. Microbes Environ 28:244–250
Im J, Lee SW, Yoon S, DiSpirito AA, Semrau JD (2011) Characterization of a novel facultative Methylocystis species capable of growth on methane, acetate and ethanol. Environ Microbiol Rep 3:174–181
Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, Suzuki M, Takai K, Delwiche M et al (2006) Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc Natl Acad Sci U S A 103:2815–2820
IPCC (2007) Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB et al (eds) contribution of working group I to the fourth assessment report of the intergovermmental panel on climate change (IPCC). Cambridge University Press, Cambridge, UK/New York
Islam T, Jensen S, Reigstad LJ, Larsen O, Birkeland NK (2008) Methane oxidation at 55 degrees C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum. Proc Natl Acad Sci U S A 105:300–304
Islas-Lima S, Thalasso F, Gómez-Hernandez J (2004) Evidence of anoxic methane oxidation coupled to denitrification. Water Res 38:13–16
Jetten MSM, Stams AJM, Zehnder AJB (1992) Methanogenesis from acetate - a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. FEMS Microbiol Rev 88:181–197
Jézéquel D, Michard G, Viollier E, Prévot F, Groleau A, Sarazin G, Lopes F (2010) Le cycle du carbone et les risques d’éruption gazeuse au Pavin. Rev Sci Nat Auver 74:67–86
Kankaala P, Taipale S, Grey J, Sonninen E, Arvola L, Jones RI (2006) Experimental delta C-13 evidence for a contribution of methane to pelagic food webs in lakes. Limnol Oceanogr 51:2821–2827
Kaserer H (1905) Ueber die oxydation des wasserstofes und des methane durch mikroorganismen (Sur l’oxydation de l’hydrogène et du méthane par les microorganismes). Z landw Versuchsw in Osterreich 8:789–792
Kiyashko SI, Imbs AB, Narita T, Svetashev VI, Wada E (2004) Fatty acid composition of aquatic insect larvae Stictochironomus pictulus (Diptera: Chironomidae): evidence of feeding upon methanotrophic bacteria. Comp Biochem Physiol B Biochem Mol Biol 139:705–711
Knittel K, Boetius A (2009) The anaerobic oxidation of methane-progress with an unknown process. Annu Rev Microbiol 63:311–334
Knittel K, Losekann T, Boetius A, Kort R, Amann R (2005) Diversity and distribution of methanotrophic archaea at cold seeps. Appl Environ Microbiol 71:467–479
Kruger M, Meyerdierks A, Glockner FO, Amann R, Widdel F, Kube M, Reinhardt R, Kahnt R, Bocher R, Thauer RK, Shima S (2003) A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426:878–881
Kvenvolden KA, Rogers BW (2005) Gaia’s breath-global methane exhalations. Mar Pet Geol 22:579–590
Lamprecht I (1980) Growth and metabolism in yeasts. In: Beezer AE (ed) Biological microcalorimetry. Academic, London, pp 43–112
Lang K, Schuldes J, Kligl A, Poehlein A, Daniel R, Brune A (2015) New mode of energy metabolism in the seventh order of methanogens as revealed by comparative genome analysis of “Candidatus Methanoplasma termitum”. Appl Environ Microbiol 81:1338–1352
Lavoisier AL, de Laplace PS (1780) Mémoire sur la chaleur. Mémoires de l’Académie des Sciences, Paris. Available online by CRHST/CNRS
Lehours AC, Bardot C, Thenot A, Debroas D, Fonty G (2005) Anaerobic microbial communities in Lake Pavin, a unique meromictic lake in France. Appl Environ Microbiol 71:7389–7400
Lehours AC, Evans P, Bardot C, Joblin K, Gerard F (2007) Phylogenetic diversity of archaea and bacteria in the anoxic zone of a meromictic lake (Lake Pavin, France). Appl Environ Microbiol 73:2016–2019
Lehours AC, Batisson I, Guedon A, Mailhot G, Fonty G (2009) Diversity of culturable bacteria, from the anaerobic zone of the meromictic lake pavin, able to perform dissimilatory-iron reduction in different in vitro conditions. Geomicrobiol J 26:212–223
Lehours AC, Rabiet M, Morel-Desrosiers N, Morel JP, Jouve L, Arbeille B, Mailhot G, Fonty G (2010) Ferric iron reduction by fermentative strain BS2 isolated from an iron-rich anoxic environment (Lake Pavin, France). Geomicrobiol J 27:714–722
Lelieved J, Crutzen PJ, Dentener FJ (1998) Changing concentration, lifetime and climate forcing of atmospheric methane. Tellus B Chem Phys Meteorol 50:128–150
Lescure T, Carpentier A, Battaglia-Brunet F, Morel-Desrosiers N (2013) Oxidation of As(III) by the bacterial community of a marine sediment monitored by microcalorimetry. Geomicrobiol J 30:540–548
Liikanen A, Martikainen PJ (2003) Effect of ammonium and oxygen on methane and nitrous oxide fluxes across sediment-water interface in a eutrophic lake. Chemosphere 52:1287–1293
Liikanen A, Huttunen JT, Valli K, Martikainen PJ (2002) Methane cycling in the sediment and water column of mid-boreal hyper-eutrophic Lake Kevätön, Finland. Arch Hydrobiol 154:585–603
Lipscomb JD (1994) Biochemistry of the soluble methane monooxygenase. Annu Rev Microbiol 48:371–399
Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stephanauskas R, Ritcher M, Kleindienst S, Lenk S, Schramm A, Jørgensen BB (2013) Predominant Archaea in marine sediments degrade detrital proteins. Nature 496:1–6
Lomans BP, Smolders AJP, Intven LM, Pol A, denCamp H, vanderDrift C (1997) Formation of dimethyl sulfide and methanethiol in anoxic freshwater sediments. Appl Environ Microbiol 63:4741–4747
Lomans BP, Luderer R, Steenbakkers P, Pol A, van der Drift C, Vogels GD, Op den Camp HJM (2001) Microbial populations involved in cycling of dimethyl sulfide and methanethiol in freshwater sediments. Appl Environ Microbiol 67:1044–1051
Lopes F, Viollier E, Thiam A, Michard G, Abril G, Groleau A, Prévot F, Carrias JF, Albéric P, Jézéquel D (2011) Biogeochemical modeling of anaerobic vs. aerobic methane oxidation in a meromictic crater lake (Lake Pavin, France). Appl Geochem 26:1919–1932
Lösekann T, Knittel K, Nadalig T, Fuchs B, Niemann H, Boetius A, Amann R (2007) Diversity and abundance of aerobic and anaerobic methane oxidizers at the Haakon Mosby Mud Volcano, Barents Sea. Appl Environ Microbiol 73:3348–3362
Lovley DR (1987) Organic matter mineralization with the reduction of ferric iron: a review. Geomicrobiol J 5:375–399
Lovley DR (2006) The dissimilatory Fe(III)- and Mn(IV)-reducing prokaryotes. The Prokaryotes, vol. 2 (Springerlink eds.), Springer, New York, pp 635–658
Lovley DR, Klug MJ (1983) Methanogenesis from methanol and methylamines and acetogenesis from hydrogen and carbon-dioxide in the sediments of a eutrophic lake. Appl Environ Microbiol 45:1310–1315
Lovley DR, Phillips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron and manganese. Appl Environ Microbiol 54:1472–1480
Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiol 148:3521–3530
Mayr S, Latkoczy C, Kruger M, Gunther D, Shima S, Thauer RK, Widdel F, Jaun B (2008) Structure of an F430 variant from archaea associated with anaerobic oxidation of methane. J Am Chem Soc 130:10758–10767
Mc Inerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM, Schink B, Rohlin L, Gunsalus RP (2008) Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann NY Acad Sci 1125:58–72
McInerney MJ, Sieber JR, Gunsalus RP (2009) Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20:623–632
McInerney MJ, Sieber JR, Gunsalus R (2011) Microbial syntrophy: ecosystem-level biochemical cooperation. Microbe 6:479–485
Michmerhuizen CM, Striegl RG, McDonald ME (1996) Potential methane emission from north-temperate lakes following ice melt. Limnol Oceanogr 41:985–991
Miller TL, Wolin MJ (1985) Methanosphaera stadtmaniae gen. nov., sp. nov.: a species that forms methane by reducing methanol with hydrogen. Arch Microbiol 141:116–122
Müller V, Imkamp F, Rauwolf A, Küsel K, Drake HL (2004) Molecular and cellular biology of acetogenic bacteria. In: Nakano MM, Zuber P (eds) Strict and facultative anaerobes: medical and environmental aspects. Horizon Bioscience, Wymondham, pp 251–281
Müller N, Griffin BM, Stingl U, Schink B (2008) Dominant sugar utilizers in sediment of Lake Constance depend on syntrophic cooperation with methanogenic partner organisms. Environ Microbiol 10:1501–1511
Murase J, Sugimoto A (2005) Inhibitory effect of light on methane oxidation in the pelagic water column of a mesotrophic lake (Lake Biwa, Japan). Limnol Oceanogr 50:1339–1343
Murase J, Sakai Y, Kametani A, Sugimoto A (2005) Dynamics of methane in mesotrophic Lake Biwa, Japan. Ecol Res 20:377–385
Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev 6:441–454
Nazaries L, Murrell JC, Millard P, Baggs L, Singh BK (2013) Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions. Environ Microbiol 15:2395–2417
Nold SC, Boschker HTS, Pel R, Laanbroek HJ (1999) Ammonium addition inhibits C-13-methane incorporation into methanotroph membrane lipids in a freshwater sediment. FEMS Microbiol Ecol 29:81–89
Nozhevnikova AN, Nekrasova V, Ammann A, Zehnder AJB, Wehrli B, Holliger C (2007) Influence of temperature and high acetate concentrations on methanogenensis in lake sediment slurries. FEMS Microbiol Ecol 62:336–344
Nüsslein B, Eckert W, Conrad R (2003) Stable isotope biogeochemistry of methane formation in profundal sediments of Lake Kinneret (Israel). Limnol Oceanogr 48:1439–1446
Ollivier B, Caumette P, Garcia JL, Mah RA (1994) Anaerobic bacteria from hypersaline environments. Microbiol Rev 58:27–38
Omil F, Lens P, Visser A, Hulshoff Pol LW, Lettinga G (1998) Long-term competition between sulfate reducing and methanogenic bacteria in UASB reactors treating volatile fatty acids. Biotechnol Bioeng 57:676–685
Op den Camp HJM, Islam T, Stott MB, Harhangi HR, Hynes A, Schouten S, Jetten MSM, Birkeland N-K, Pol A, Dunfield PF (2009) Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 1:293–306
Oremland RS, Polcin S (1982) Methanogenesis and sulfate reduction: competitive and noncompetitive substrates in estuarine sediments. Appl Environ Microbiol 44:1270–1276
Orphan VJ, House CH, Hinrichs KU, McKeegan KD, DeLong EF (2001) Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293:484–487
Patel GB, Sprott GD (1990) Methanosaeta concilii gen. nov., sp. nov. (“Methanothrix concilii”) and Methanosaeta thermoacetophila nom. rev., comb. nov. Int J Syst Bacteriol 40:79–82
Paul K, Nonoh JO, Mikulski L, Brune A (2012) “Methanoplasmatales”, Thermoplasmatales-related archaea in termite guts and other environments, are the seventh order of methanogens. Appl Environ Microbiol 78:8245–8253
Pavlov AA, Kasting JF, Brown LL, Rages KA, Freedman R (2000) Greenhouse warming by CH4 in the atmosphere of early Earth. J Geophys Res 105:11981–11990
Pernthaler A, Orphan VJ (2010) U.S. Patent No. 7736855. Process for separating microorganisms. U.S. Patent and Trademark Office, Washington, DC
Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68:3094–3101
Pernthaler A, Dekas AE, Brown CT, Goffredi SK, Embaye T, Orphan VJ (2008) Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics. Proc Natl Acad Sci U S A 105:7052–7057
Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MSM, den Camp H (2007) Methanotrophy below pH1 by a new Verrucomicrobia species. Nature 450:817–874
Poulsen M, Schwab C, Jensen BB, Engberg RM, Spang A, Canibe N, Højberg O, Milinovich G, Fragner L, Schleper C, Weckwerth W, Lund P, Schramm A, Urich T (2013) Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat Commun 4:1428
Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KF, Rijpstra WIC, Schouten S, Damste JSS, Op den Camp HJM et al (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440:918–921
Ragsdale SW, Kumar M (1996) Nickel-containing carbon monoxide dehydrogenase/acetyl-CoA synthase. Chem Rev 96:2515–2539
Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood-Ljundahl pathway of CO2 fixation. Biochim Biophys Acta 1784:1873–1898
Ravussin E, Burnand B, Schutz Y, Jéquier E (1982) Twenty-four-hour energy expenditure and resting metabolic rate in obese, moderately obeses and control subjects. Am J Clin Nutr 35:566–573
Reeburgh WS (2003) Global methane biogeochemistry. In: Keeling RF, Holland HD, Turekian KK (eds) Treatise on geochemistry, vol 4, The atmosphere. Elsevier-Pergamon, Oxford, pp 65–89
Scheller S, Goenrich M, Boecher R, Thauer RK, Jaun B (2010) The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane. Nature 465:606–608
Schimel J (2004) Playing scales in the methane cycle: from microbial ecology to the globe. Proc Natl Acad Sci USA 101:12400–12401
Schink B (1997) Energetics of syntrophic cooperations in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280
Schink B, Stams AJM (2001) Syntrophism among prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: an evolving electronic resource for the microbiological community, 3rd edn. Springer, New York, p 25
Schonheit P, Keweloh H, Thauer RK (1981) Factor F420 degradation in Methanobacterium thermoautotrophicum during exposure to oxygen. FEMS Microbiol Lett 12:347–349
Schubert CJ, Vazquez F, Lösekann-Behrens T, Knittel K, Tonolla M, Boetius A (2011) Evidence for anaerobic oxidation of methane in sediments of a freshwater system (Lago di Cadagno). FEMS Microbiol Ecol 76:26–38
Schulz S, Conrad R (1996) Influence of temperature on pathways to methane production in the permanently cold profundal sediment of Lake Constance. FEMS Microbiol Ecol 20:1–14
Shindell DT, Faluvegi G, Koch DM, Schmidt GA, Unger N, Bauer SE (2009) Improved attribution of climate forcing to emissions. Science 326:716–718
Sieber JR, McInerney MJ, Gunsalus RP (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66:429–452
Smith KS, Ingram-Smith C (2007) Methanosaeta, the forgotten methanogen? Trends Microbiol 15:150–155
Smith RL, Howes BL, Garabedian SP (1991) In situ measurement of methane oxidation in groundwater by using natural-gradient tracer tests. Appl Environ Microbiol 57:1997–2004
Sohngen NL (1906) Uber bakterien welche methan ab kohlenstoffnahrung und energiequelle gerbrauchen (Les bactéries qui utilisent le méthane comme source d’énergie et de carbone). Z Bakteriol Parazitenk (Infektionster) 15:513–517
Sprenger WW, van Belzen MC, Rosenberg J, Hackstein JHP, Keltjens JT (2000) Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. Int J Syst Evol Microbiol 50:1989–1999
Sprenger WW, Hackstein JHP, Keltjens JT (2005) The energy metabolism of Methanomicrococcus blatticola: physiological and biochemical aspects. Antonie Van Leeuwenhoek 87:289–299
Stams AJM, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568e577
Stephenson M (1947) Some aspects of hydrogen transfer. Ant v Leeuwenhoek 12:33–48
Stoecker K, Bendinger B, Schoning B, Nielsen PH, Nielsen JL, Baranyi C, Toenshoff ER, Daims H, Wagner M (2006) Cohn’s Crenothrix is a filamentous methane oxidizer with an unusual methane monooxygenase. Proc Natl Acad Sci U S A 103:2363–2367
Tewes FJ, Thauer RK (1980) Regulation of ATP synthesis in glucose fermenting bacteria involved in interspecies hydrogen transfer. In: Gottschalk G, Pfennig N, Werner H (eds) Anaerobes and anaerobic infections. G. Fischer, Stuttgart, pp 97–104
Thauer RK, Shima S (2008) Methane as fuel for anaerobic microorganisms. Ann NY Acad Sci 1125:158–170
Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591
Trembath-Reichert E, Green-Saxena A, Orphan VJ (2013) Whole cell immunomagnetic enrichment of environmental microbial consortia using rRNA-targeted Magneto-FISH. Methods Enzymol 531:21–44
Trotsenko YA, Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 63:183–229
Van Bodegom PM, Scholten JCM, Roden EE, Stams AJM (2004) Direct inhibition of methanogenesis by ferric iron. FEMS Microb Ecol 49:261–268
Von Stockar U, Marison IW (1989) The use of calorimetry in biotechnology. In: Fiechter A (ed) Advances in biochemical engineering/biotechnology, vol 40. Springer, Berlin, pp 93–134
Wadsö I (1985) Isothermal biocalorimetry. A status report. Thermochimica Acta 88:35–48
Wang JS, Logan JA, McElroy MB, Duncan BN, Megretskaia IA, Yantosca RM (2004) A 3-D model analysis of the slowdown and interannual variability in the methane growth rate from 1988 to 1997. Global Biogeochem Cycles 18:B3011. doi:10.1029/2003GB002180
Webster G, Sass H, Cragg BA, Gorra R, Knab NJ, Green CJ, Mathes F, Fry JC, Weightman AJ et al (2011) Enrichment and cultivation of prokaryotes associated with the sulphate methane transition zone of diffusion controlled sediments of Aarhus Bay, Denmark under heterotrophic conditions. FEMS Microbiol Ecol 77:248–263
Wetzel RG (2001) Limnology – Lake and river ecosystems, 3rd edn. Academic, San Diego, p 1006
Whiticar MJ (1999) Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chem Geol 16:1291–1314
Widdel F (1988) Microbiology and ecology of sulfate- and sulfur-reducing bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 469–585
Ye WJ, Liu XL, Lin SQ, Tan J, Pan JL, Li DT, Yang H (2009) The vertical distribution of bacterial and archaeal communities in the water and sediment of Lake Taihu. FEMS Microbiol Ecol 70:263–276
Yvon-Durocher G, Allen AP, Batsviken D, Conrad R, Gudasz C, St-Pierr A, Thanh-Duc N, del Giorgio P (2014) Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507:488–491
Zeikus JG (1977) The biology of methanogenic bacteria. Bacteriol Rev 41:514–541
Zeikus, JG (1983) Metabolic communication between biodegradative populations in nature. In: Slater JH, Whittenbury R, Wimpenny, JWT (eds) Microbes in their natural environments. Soc Gen Microbiol Symp 34:423–462. Cambridge, UK: Cambridge University Press
Zhang Y, Maignien L, Zhao X, Wang F, Boon N (2011) Enrichment of a microbial community performing anaerobic oxidation of methane in a continuous high-pressure bioreactor. BMC Microbiol 11:137–145
Zinder SH (1993) Physiological ecology of methanogens. In: Ferry JG (ed) Methanogenesis. Chapman & Hall, New York, pp 128–206
Zinder SH, Brock TD (1978) Production of methane and carbon dioxide from methane thiol and dimethyl sulfide by anaerobic lake-sediments. Nature 273:226–228
Zumft WG (1992) The denitrifying prokaryotes. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, New York, pp 554–582
Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616
Acknowledgements
This study includes results from Master, PhD and postdoc researches supported by various instances: Région Auvergne, CNRS, Université Blaise Pascal, Ministère de la Recherche et de la Technologie. Part of the results presented was obtained with the collaboration of colleagues: Didier Jézéquel, Gilles Mailhot, Jonathan Colombet, Keith Joblin, Paul Evans, Annie Guedon, Corinne Biderre-Petit, Marion Rabiet, Karl Rockne, Christophe Guimbaud, Frédéric Savoie, Stéphane Chevrier, Pierre Agrinier, Nelly Assayag, François Prévot, Jean-Claude Romagoux, Guy Demeure, Aurélie Thénot, Télesphore Sime-Ngando. The studies were granted from different sources: French National Program EC2CO (Projects INTERLAC, METHANOLAC) and ANR Program (Project METANOX). We thank the reviewer, Bernard Ollivier, for his constructive comments, which helped us to improve the manuscript.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Lehours, AC. et al. (2016). Anaerobic Microbial Communities and Processes Involved in the Methane Cycle in Freshwater Lakes-a Focus on Lake Pavin. In: Sime-Ngando, T., Boivin, P., Chapron, E., Jezequel, D., Meybeck, M. (eds) Lake Pavin. Springer, Cham. https://doi.org/10.1007/978-3-319-39961-4_16
Download citation
DOI: https://doi.org/10.1007/978-3-319-39961-4_16
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-39960-7
Online ISBN: 978-3-319-39961-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)