Anaerobic Oxidation of Methane in Sediments of Lake Constance, an Oligotrophic Freshwater Lake

ABSTRACT Anaerobic oxidation of methane (AOM) with sulfate as terminal electron acceptor has been reported for various environments, including freshwater habitats, and also, nitrate and nitrite were recently shown to act as electron acceptors for methane oxidation in eutrophic freshwater habitats. Radiotracer experiments with sediment material of Lake Constance, an oligotrophic freshwater lake, were performed to follow 14CO2 formation from 14CH4 in sediment incubations in the presence of different electron acceptors, namely, nitrate, nitrite, sulfate, or oxygen. Whereas 14CO2 formation without and with sulfate addition was negligible, addition of nitrate increased 14CO2 formation significantly, suggesting that AOM could be coupled to denitrification. Nonetheless, denitrification-dependent AOM rates remained at least 1 order of magnitude lower than rates of aerobic methane oxidation. Using molecular techniques, putative denitrifying methanotrophs belonging to the NC10 phylum were detected on the basis of the pmoA and 16S rRNA gene sequences. These findings show that sulfate-dependent AOM was insignificant in Lake constant sediments. However, AOM can also be coupled to denitrification in this oligotrophic freshwater habitat, providing first indications that this might be a widespread process that plays an important role in mitigating methane emissions.

[1]  Jonathan J. Cole,et al.  Methane emissions from lakes: Dependence of lake characteristics, two regional assessments, and a global estimate , 2004 .

[2]  U. Stingl,et al.  Dominant sugar utilizers in sediment of Lake Constance depend on syntrophic cooperation with methanogenic partner organisms. , 2008, Environmental microbiology.

[3]  李幼升,et al.  Ph , 1989 .

[4]  K. Timmis.  Handbook of hydrocarbon and lipid microbiology , 2010 .

[5]  Olaf Pfannkuche,et al.  A marine microbial consortium apparently mediating anaerobic oxidation of methane , 2000, Nature.

[6]  J. Yavitt,et al.  Anaerobic oxidation of methane: an underappreciated aspect of methane cycling in peatland ecosystems? , 2011 .

[7]  Seigo Shima,et al.  Methane as Fuel for Anaerobic Microorganisms , 2008, Annals of the New York Academy of Sciences.

[8]  K. Nauhaus,et al.  In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate. , 2007, Environmental microbiology.

[9]  P. Bottner,et al.  Comparison of five soil organic matter decomposition models using data from a 14C and 15N labeling field experiment , 2004 .

[10]  K. Knittel,et al.  Anaerobic oxidation of methane: progress with an unknown process. , 2009, Annual review of microbiology.

[11]  S. P. Garabedian,et al.  In situ measurement of methane oxidation in groundwater by using natural-gradient tracer tests , 1991, Applied and environmental microbiology.

[12]  B. Schink.  Energetics of syntrophic cooperation in methanogenic degradation , 1997, Microbiology and molecular biology reviews : MMBR.

[13]  R. Amann,et al.  Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group. , 2010, Environmental microbiology.

[14]  O. Edenhofer,et al.  Mitigation from a cross-sectoral perspective , 2007 .

[15]  R. Conrad,et al.  Effects of nitrate, nitrite, NO and N2O on methanogenesis and other redox processes in anoxic rice field soil , 1998 .

[16]  S. Solomon.  The Physical Science Basis : Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change , 2007 .

[17]  Ming L. Wu,et al.  Nitrite-driven anaerobic methane oxidation by oxygenic bacteria , 2010, Nature.

[18]  B. Schink,et al.  Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. , 2004, FEMS microbiology ecology.

[19]  Mike S. M. Jetten,et al.  A microbial consortium couples anaerobic methane oxidation to denitrification , 2006, Nature.

[20]  Bernhard Schink,et al.  Activity and Diversity of Methanotrophic Bacteria at Methane Seeps in Eastern Lake Constance Sediments , 2011, Applied and Environmental Microbiology.

[21]  J. Yavitt,et al.  Evidence for Anaerobic CH 4 Oxidation in Freshwater Peatlands , 2007 .

[22]  Daniel Rokhsar,et al.  Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics , 2004, Science.

[23]  I. Bussmann,et al.  Methane Release through Resuspension of Littoral Sediment , 2005 .

[24]  B. Schink,et al.  Abundance and Activity of Methanotrophic Bacteria in Littoral and Profundal Sediments of Lake Constance (Germany) , 2008, Applied and Environmental Microbiology.

[25]  F Thalasso,et al.  Evidence of anoxic methane oxidation coupled to denitrification. , 2004, Water research.

[26]  H. Cypionka,et al.  Life at the oxic-anoxic interface: microbial activities and adaptations. , 2000, FEMS microbiology reviews.

[27]  R. Zeng,et al.  Effect of nitrate and nitrite on the selection of microorganisms in the denitrifying anaerobic methane oxidation process. , 2011, Environmental microbiology reports.

[28]  M. Kimura,et al.  Methane Production and Its Fate in Paddy Fields : I. Effects of Rice Straw Application and Percolation Rate on the Leaching of Methane and Other Soil Components into the Subsoil , 1992 .

[29]  M. Kimura,et al.  Methane production and its fate in paddy fields VII. Electron acceptors responsible for anaerobic methane oxidation , 1994 .

[30]  Y. Koizumi,et al.  Characterization of depth-related microbial community structure in lake sediment by denaturing gradient gel electrophoresis of amplified 16S rDNA and reversely transcribed 16S rRNA fragments. , 2003, FEMS microbiology ecology.

[31]  Thomas E Hanson,et al.  Methanotrophic bacteria. , 1996, Microbiological reviews.

[32]  M. Kimura,et al.  Methane production and its fate in paddy fields. VI: Anaerobic oxidation of methane in plow layer soil , 1994 .

[33]  M. Krüger,et al.  Cooccurrence of Aerobic and Anaerobic Methane Oxidation in the Water Column of Lake Plußsee , 2005, Applied and Environmental Microbiology.

[34]  Corinne Le Quéré,et al.  Climate Change 2013: The Physical Science Basis , 2013 .

[35]  Jens Harder,et al.  Anaerobic methane oxidation by bacteria employing 14C-methane uncontaminated with 14C-carbon monoxide , 1997 .

[36]  B. Schink,et al.  Methanogenic degradation of acetone by an enrichment culture , 2004, Archives of Microbiology.

[37]  Thomas D. Brock,et al.  Anaerobic Methane Oxidation: Occurrence and Ecology , 1980, Applied and environmental microbiology.

[38]  A Costello,et al.  Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. , 1995, FEMS microbiology letters.

[39]  B. Schink,et al.  Cultivation of methanotrophic bacteria in opposing gradients of methane and oxygen. , 2006, FEMS microbiology ecology.

[40]  C. Yin,et al.  Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems , 2010, Applied Microbiology and Biotechnology.

[41]  Ming L. Wu,et al.  Physiological role of the respiratory quinol oxidase in the anaerobic nitrite-reducing methanotroph 'Candidatus Methylomirabilis oxyfera'. , 2011, Microbiology.

[42]  V. Orphan,et al.  Manganese- and Iron-Dependent Marine Methane Oxidation , 2009, Science.

[43]  K. Nauhaus,et al.  In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. , 2002, Environmental microbiology.

[44]  R. Zeng,et al.  Enrichment of denitrifying anaerobic methane oxidizing microorganisms. , 2009, Environmental microbiology reports.

[45]  Mike S. M. Jetten,et al.  Enrichment and Molecular Detection of Denitrifying Methanotrophic Bacteria of the NC10 Phylum , 2009, Applied and Environmental Microbiology.

[46]  B. Wehrli,et al.  Extreme methane emissions from a Swiss hydropower reservoir: contribution from bubbling sediments. , 2010, Environmental science & technology.

[47]  William R. Taylor,et al.  The rapid generation of mutation data matrices from protein sequences , 1992, Comput. Appl. Biosci..

[48]  M. Strous.  Global Consequences of Anaerobic Methane Oxidation , 2010 .

[49]  G. King.  Ecological Aspects of Methane Oxidation, a Key Determinant of Global Methane Dynamics , 1992 .

[50]  H. L. Miller,et al.  Climate Change 2007: The Physical Science Basis , 2007 .

[51]  N. Pfennig,et al.  Acetylene inhibition technique underestimates in situ denitrification rates in intact cores of freshwater sediment , 1991 .

[52]  B. Schink,et al.  Dynamics in composition and size-class distribution of humic substances in profundal sediments of Lake Constance , 2001 .

[53]  Rudolf Amann,et al.  A conspicuous nickel protein in microbial mats that oxidize methane anaerobically , 2003, Nature.

[54]  Marnix H Medema,et al.  Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. , 2008, Environmental microbiology.

[55]  A. Zehnder,et al.  Measuring Radioactive Methane with the Liquid Scintillation Counter , 1979, Applied and Environmental Microbiology.

[56]  A. Zehnder,et al.  Methane formation and methane oxidation by methanogenic bacteria , 1979, Journal of bacteriology.

[57]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[58]  F. Widdel.  Growth of Methanogenic Bacteria in Pure Culture with 2-Propanol and Other Alcohols as Hydrogen Donors , 1986, Applied and environmental microbiology.

[59]  A. Chao.  Estimating the population size for capture-recapture data with unequal catchability. , 1987, Biometrics.

[60]  D. Valentine,et al.  New perspectives on anaerobic methane oxidation. , 2000, Environmental microbiology.

[61]  Peter G. Brewer,et al.  Methane-consuming archaebacteria in marine sediments , 1999, Nature.

[62]  Tori M. Hoehler,et al.  Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen‐sulfate reducer consortium , 1994 .

[63]  I. Cozzarelli,et al.  Anaerobic methane oxidation in a landfill-leachate plume. , 2002, Environmental science & technology.

[64]  Katharine Hayhoe,et al.  Atmospheric methane and global change , 2002 .

[65]  R. Conrad,et al.  The global methane cycle: recent advances in understanding the microbial processes involved. , 2009, Environmental microbiology reports.

[66]  M. Rahalkar,et al.  Aerobic methanotrophic bacterial communities in sediments of Lake Constance , 2006 .