Methane oxidation pathways and associated methanotrophic communities in the water column of a tropical lake

We examined methane (CH4) oxidation pathways and associated methanotrophic communities in the water column of Lake Kivu using abundance and isotopic compositions of CH4 and phospholipid fatty acids (PLFA), distributions of glycerol dialkyl glycerol tetraethers, and catalyzed reporter deposition fluorescence in situ hybridization (CARD–FISH) analysis. The carbon isotopic data of CH4 indicate that aerobic CH4 oxidation is the predominant pathway of microbial CH4 consumption with an isotopic fractionation factor (α) of 1.022–1.038. A small amount of CH4 is oxidized anaerobically, with an α of 1.002–1.006. Aerobic CH4 oxidation is mediated by type II methane–oxidizing bacteria (type II MOB) based on the 13C depletion (δ13C of −40.5‰ to −43.7‰) of diagnostic C18:1ω7 fatty acids in the surface waters. CARD–FISH images and PLFA components C16:1ω7 and C16:1ω5 indicate the presence of type I MOB in the methane and nutrient–rich deep–water region. 13C depletion of C16:1ω7 and C16:1ω5 (δ13C, ∼ −40‰ to −50.6‰) in the lake water below 52 m suggests the involvement of type I MOB in methane oxidation in the anoxic deep–water regions of the lake. A novel cluster of anaerobic methane–oxidizing archaea (ANME) rather than the known ANME–1 and ANME–2 appear to be involved in anaerobic oxidation of methane (AOM). Sulfate reducing bacteria are associated with AOM in the lake based on the 13C depletion (δ13C, −38.2‰ to −45.0‰) of anteiso–methyl–C15:0 fatty acid. Methane constitutes an important carbon and energy source (up to 38%) for the heterotrophic and autotrophic communities in the lake.

[1]  A. Borges,et al.  Biogeochemistry of a large and deep tropical lake (Lake Kivu, East Africa: insights from a stable isotope study covering an annual cycle , 2014 .

[2]  J. Downing,et al.  Stable carbon isotope biogeochemistry of lakes along a trophic gradient , 2014 .

[3]  A. Borges,et al.  Biogeochemistry of a large, meromictic tropical lake (Lake Kivu, East Africa): insights from a stable isotope study covering an annual cycle , 2014 .

[4]  Shihu Hu,et al.  Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage , 2013, Nature.

[5]  W. Ussler,et al.  Abundance and distribution of diverse membrane-bound monooxygenase (Cu-MMO) genes within the Costa Rica oxygen minimum zone. , 2013, Environmental microbiology reports.

[6]  Markus Schmid,et al.  Zero-valent sulphur is a key intermediate in marine methane oxidation , 2012, Nature.

[7]  H. Sarmento,et al.  Phytoplankton of Lake Kivu , 2012 .

[8]  M. Schmid,et al.  Lake Kivu Research: Conclusions and Perspectives , 2012 .

[9]  B. Delille,et al.  Diffusive methane emissions to the atmosphere from Lake Kivu (Eastern Africa) , 2011 .

[10]  H. Bürgmann,et al.  Methane sources and sinks in Lake Kivu , 2011 .

[11]  E. Casamayor,et al.  Active bacteria and archaea cells fixing bicarbonate in the dark along the water column of a stratified eutrophic lagoon. , 2011, FEMS microbiology ecology.

[12]  M. Schmid,et al.  What prevents outgassing of methane to the atmosphere in Lake Tanganyika , 2011 .

[13]  K. Knittel,et al.  Evidence for anaerobic oxidation of methane in sediments of a freshwater system (Lago di Cadagno). , 2011, FEMS microbiology ecology.

[14]  S. Katsev,et al.  The methane cycle in ferruginous Lake Matano , 2011, Geobiology.

[15]  E. Casamayor,et al.  Vertical Distribution of Ammonia-Oxidizing Crenarchaeota and Methanogens in the Epipelagic Waters of Lake Kivu (Rwanda-Democratic Republic of the Congo) , 2010, Applied and Environmental Microbiology.

[16]  T. Diem,et al.  Oxidation and emission of methane in a monomictic lake (Rotsee, Switzerland) , 2010, Aquatic Sciences.

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

[18]  A. Wüest,et al.  Physical and biogeochemical limits to internal nutrient loading of meromictic Lake Kivu , 2009 .

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

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

[21]  J. S. Sinninghe Damsté,et al.  Tetraether membrane lipid distributions in water-column particulate matter and sediments: a study of 47 European lakes along a north–south transect , 2009 .

[22]  J. Damsté,et al.  A reanalysis of phospholipid fatty acids as ecological biomarkers for methanotrophic bacteria , 2009, The ISME Journal.

[23]  H. Niemann,et al.  Diagnostic lipid biomarker and stable carbon isotope signatures of microbial communities mediating the anaerobic oxidation of methane with sulphate , 2008 .

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

[26]  P. Giorgio,et al.  Direct measurement of the d13C signature of carbon respired by bacteria in lakes: Linkages to potential carbon sources, ecosystem baseline metabolism, and CO2 fluxes , 2008 .

[27]  H. Nykänen,et al.  Oxidation, efflux, and isotopic fractionation of methane during autumnal turnover in a polyhumic, boreal lake , 2007 .

[28]  W. Reeburgh.  Oceanic methane biogeochemistry. , 2007, Chemical reviews.

[29]  L. Alvarez-Cohen,et al.  Variable carbon isotope fractionation expressed by aerobic CH4-oxidizing bacteria , 2006 .

[30]  Martin Schmid,et al.  Weak mixing in Lake Kivu: New insights indicate increasing risk of uncontrolled gas eruption , 2005 .

[31]  T. Treude,et al.  Anaerobic oxidation of methane and sulfate reduction along the Chilean continental margin , 2005 .

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

[33]  R. Seifert,et al.  Membrane lipid patterns typify distinct anaerobic methanotrophic consortia. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  L. Tranvik,et al.  Methane as a source of carbon and energy for lake pelagic food webs , 2003 .

[35]  J. S. Sinninghe Damsté,et al.  Molecular isotopic tracing of carbon flow and trophic relationships in a methane‐supported benthic microbial community , 2002 .

[36]  P. Frenzel,et al.  Changes in Activity and Community Structure of Methane-Oxidizing Bacteria over the Growth Period of Rice , 2001, Applied and Environmental Microbiology.

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

[38]  R. Pancost,et al.  Biomarker Evidence for Widespread Anaerobic Methane Oxidation in Mediterranean Sediments by a Consortium of Methanogenic Archaea and Bacteria , 2000, Applied and Environmental Microbiology.

[39]  Michael J. Whiticar,et al.  Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane , 1999 .

[40]  K. Schleifer,et al.  The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. , 1999, Systematic and applied microbiology.

[41]  H. Schulz,et al.  Stable phytoplankton community structure in the Arabian Sea over the past 200,000 years , 1998, Nature.

[42]  R. Knowles,et al.  Growth of methanotrophs in methane and oxygen counter gradients , 1995 .

[43]  R. Summons,et al.  Carbon isotopic fractionation in lipids from methanotrophic bacteria: relevance for interpretation of the geochemical record of biomarkers. , 1994, Geochimica et cosmochimica acta.

[44]  D. Stahl,et al.  Comparison of phylogenetic relationships based on phospholipid fatty acid profiles and ribosomal RNA sequence similarities among dissimilatory sulfate-reducing bacteria. , 1994, FEMS microbiology letters.

[45]  J. Hayes.  Factors controlling 13C contents of sedimentary organic compounds: Principles and evidence , 1993 .

[46]  M. Lidstrom,et al.  Seasonal Study of Methane Oxidation in Lake Washington , 1984, Applied and environmental microbiology.

[47]  H. Jannasch.  Methane oxidation in Lake Kivu (central Africa)1 , 1975 .

[48]  Stefan Schouten,et al.  The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: A review , 2013 .

[49]  B. Wehrli,et al.  Submicromolar Oxygen Profiles at the Oxic–Anoxic Boundary of Temperate Lakes , 2013, Aquatic Geochemistry.

[50]  Muvundja Amisi,et al.  RIVERINE NUTRIENT INPUTS TO LAKE KIVU , 2010 .

[51]  S. L. McCallister.  Direct measurement of the d 13 C signature of carbon respired by bacteria in lakes : Linkages to potential carbon sources , ecosystem baseline metabolism , and CO 2 fluxes , 2008 .

[52]  Methane oxidation in Lake Kivu ( central Africa ) , 2000 .

[53]  D. D. Marais,et al.  Carbon isotopic fractionation in lipids from methanotrophic bacteria II: the effects of physiology and environmental parameters on the biosynthesis and isotopic signatures of biomarkers. , 1999, Geochimica et cosmochimica acta.

[54]  S. Wakeham,et al.  Compositions and transport of lipid biomarkers through the water column and surficial sediments of the equatorial Pacific Ocean , 1997 .

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

[56]  R. Amann,et al.  Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. , 1993, Cytometry.

[57]  David A. Stahl,et al.  Development and application of nucleic acid probes , 1991 .