An evolving view of methane metabolism in the Archaea

Evans, Paul N.; Boyd, Joel A.; Leu, Andy O.; Woodcroft, Ben J.; Parks, Donovan H.; Hugenholtz, Philip; Tyson, Gene W.

doi:10.1038/s41579-018-0136-7

An evolving view of methane metabolism in the Archaea

Journal Article · Mon Jan 21 04:00:00 EST 2019 · Nature Reviews Microbiology

DOI:https://doi.org/10.1038/s41579-018-0136-7· OSTI ID:1856863

Evans, Paul N. ^[1]; Boyd, Joel A. ^[2]; Leu, Andy O. ^[2]; Woodcroft, Ben J. ^[2]; ^[2]; Hugenholtz, Philip ^[2]; ^[2]

Univ. of Queensland, St. Lucia, QLD (Australia); Queensland University of Technology
Univ. of Queensland, St. Lucia, QLD (Australia)

Methane is a key compound in the global carbon cycle that influences both nutrient cycling and the Earth’s climate. A limited number of microorganisms control the flux of biologically generated methane, including methane-metabolizing archaea that either produce or consume methane. Methanogenic and methanotrophic archaea belonging to the phylum Euryarchaeota share a genetically similar, interrelated pathway for methane metabolism. The key enzyme in this pathway, the methyl-coenzyme M reductase (Mcr) complex, catalyses the last step in methanogenesis and the first step in methanotrophy. Here, the discovery of mcr and divergent mcr-like genes in new euryarchaeotal lineages and novel archaeal phyla challenges long-held views of the evolutionary origin of this metabolism within the Euryarchaeota. Divergent mcr-like genes have recently been shown to oxidize short-chain alkanes, indicating that these complexes have evolved to metabolize substrates other than methane. In this Review, we examine the diversity, metabolism and evolutionary history of mcr-containing archaea in light of these recent discoveries.

Research Organization:: Univ. of Queensland, St. Lucia, QLD (Australia)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

DOE Contract Number:: SC0016440

OSTI ID:: 1856863

Journal Information:: Nature Reviews Microbiology, Journal Name: Nature Reviews Microbiology Journal Issue: 4 Vol. 17; ISSN 1740-1526

Publisher:: Springer Nature

Country of Publication:: United States

Language:: English

References (126)

Methanogenic archaea: ecologically relevant differences in energy conservation Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1931	journal	June 2008
Methanogens: a window into ancient sulfur metabolism Liu, Yuchen; Beer, Laura L.; Whitman, William B. Trends in Microbiology, Vol. 20, Issue 5 https://doi.org/10.1016/j.tim.2012.02.002	journal	May 2012
Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces Dridi, B.; Fardeau, M. -L.; Ollivier, B. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 8 https://doi.org/10.1099/ijs.0.033712-0	journal	August 2012
Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases Müller, Albert Leopold; Kjeldsen, Kasper Urup; Rattei, Thomas The ISME Journal, Vol. 9, Issue 5 https://doi.org/10.1038/ismej.2014.208	journal	October 2014
The Reaction Mechanism of Methyl-Coenzyme M Reductase: HOW AN ENZYME ENFORCES STRICT BINDING ORDER Wongnate, Thanyaporn; Ragsdale, Stephen W. Journal of Biological Chemistry, Vol. 290, Issue 15 https://doi.org/10.1074/jbc.M115.636761	journal	February 2015
Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea Hallam, S. J.; Girguis, P. R.; Preston, C. M. Applied and Environmental Microbiology, Vol. 69, Issue 9 https://doi.org/10.1128/AEM.69.9.5483-5491.2003	journal	September 2003
The energy conserving methyltetrahydromethanopterin:coenzyme M methyltransferase complex from methanogenic archaea: function of the subunit MtrH Hippler, Birgit; Thauer, Rudolf K. FEBS Letters, Vol. 449, Issue 2-3 https://doi.org/10.1016/S0014-5793(99)00429-9	journal	April 1999
The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor Cord-Ruwisch, Ralf; Seitz, Hans-J�rgen; Conrad, Ralf Archives of Microbiology, Vol. 149, Issue 4 https://doi.org/10.1007/BF00411655	journal	February 1988
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
Membrane-Bound Electron Transport in Methanosaeta thermophila Welte, C.; Deppenmeier, U. Journal of Bacteriology, Vol. 193, Issue 11 https://doi.org/10.1128/JB.00162-11	journal	April 2011
Methane-consuming archaebacteria in marine sediments Hinrichs, Kai-Uwe; Hayes, John M.; Sylva, Sean P. Nature, Vol. 398, Issue 6730 https://doi.org/10.1038/19751	journal	April 1999
Manganese- and Iron-Dependent Marine Methane Oxidation Beal, E. J.; House, C. H.; Orphan, V. J. Science, Vol. 325, Issue 5937 https://doi.org/10.1126/science.1169984	journal	July 2009
Phylogenomic Data Support a Seventh Order of Methylotrophic Methanogens and Provide Insights into the Evolution of Methanogenesis Borrel, Guillaume; O’Toole, Paul W.; Harris, Hugh M. B. Genome Biology and Evolution, Vol. 5, Issue 10 https://doi.org/10.1093/gbe/evt128	journal	August 2013
New Mode of Energy Metabolism in the Seventh Order of Methanogens as Revealed by Comparative Genome Analysis of “Candidatus Methanoplasma termitum” Lang, Kristina; Schuldes, Jörg; Klingl, Andreas Applied and Environmental Microbiology, Vol. 81, Issue 4 https://doi.org/10.1128/AEM.03389-14	journal	December 2014
Cas9-mediated genome editing in the methanogenic archaeon Methanosarcina acetivorans Nayak, Dipti D.; Metcalf, William W. Proceedings of the National Academy of Sciences, Vol. 114, Issue 11 https://doi.org/10.1073/pnas.1618596114	journal	March 2017
Taxonomic, Phylogenetic, and Ecological Diversity of Methanogenic Archaea Garcia, Jean-Louis; Patel, Bharat K. C.; Ollivier, Bernard Anaerobe, Vol. 6, Issue 4 https://doi.org/10.1006/anae.2000.0345	journal	August 2000
Metabolic, Phylogenetic, and Ecological Diversity of the Methanogenic Archaea Liu, Yuchen; Whitman, William B. Annals of the New York Academy of Sciences, Vol. 1125, Issue 1 https://doi.org/10.1196/annals.1419.019	journal	March 2008
Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments Biddle, Jennifer F.; Cardman, Zena; Mendlovitz, Howard The ISME Journal, Vol. 6, Issue 5 https://doi.org/10.1038/ismej.2011.164	journal	November 2011
Diversity and Structure of the Methanogenic Community in Anoxic Rice Paddy Soil Microcosms as Examined by Cultivation and Direct 16S rRNA Gene Sequence Retrieval Großkopf, Regine; Janssen, Peter H.; Liesack, Werner Applied and Environmental Microbiology, Vol. 64, Issue 3 https://doi.org/10.1128/AEM.64.3.960-969.1998	journal	January 1998
Zero-valent sulphur is a key intermediate in marine methane oxidation Milucka, Jana; Ferdelman, Timothy G.; Polerecky, Lubos Nature, Vol. 491, Issue 7425 https://doi.org/10.1038/nature11656	journal	November 2012
Methanobacterium lacus sp. nov., isolated from the profundal sediment of a freshwater meromictic lake Borrel, G.; Joblin, K.; Guedon, A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 7 https://doi.org/10.1099/ijs.0.034538-0	journal	September 2011
Loss of the mtr operon in Methanosarcina blocks growth on methanol, but not methanogenesis, and reveals an unknown methanogenic pathway Welander, P. V.; Metcalf, W. W. Proceedings of the National Academy of Sciences, Vol. 102, Issue 30 https://doi.org/10.1073/pnas.0502623102	journal	July 2005
Anaerobic microbial metabolism can proceed close to thermodynamic limits Jackson, Bradley E.; McInerney, Michael J. Nature, Vol. 415, Issue 6870 https://doi.org/10.1038/415454a	journal	January 2002
Rooting the Domain Archaea by Phylogenomic Analysis Supports the Foundation of the New Kingdom Proteoarchaeota Petitjean, Céline; Deschamps, Philippe; López-García, Purificación Genome Biology and Evolution, Vol. 7, Issue 1 https://doi.org/10.1093/gbe/evu274	journal	December 2014
Occurrence and expression of novel methyl-coenzyme M reductase gene (mcrA) variants in hot spring sediments McKay, Luke J.; Hatzenpichler, Roland; Inskeep, William P. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07354-x	journal	August 2017
Evolution of Na ⁺ and H ⁺ bioenergetics in methanogenic archaea Schlegel, Katharina; Müller, Volker Biochemical Society Transactions, Vol. 41, Issue 1 https://doi.org/10.1042/BST20120294	journal	February 2013
Promiscuous archaeal ATP synthase concurrently coupled to Na+ and H+ translocation Schlegel, K.; Leone, V.; Faraldo-Gomez, J. D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 3 https://doi.org/10.1073/pnas.1115796109	journal	January 2012
Single cell activity reveals direct electron transfer in methanotrophic consortia McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P. Nature, Vol. 526, Issue 7574 https://doi.org/10.1038/nature15512	journal	September 2015
Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea Nelson-Sathi, S.; Dagan, T.; Landan, G. Proceedings of the National Academy of Sciences, Vol. 109, Issue 50 https://doi.org/10.1073/pnas.1209119109	journal	November 2012
Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments Kubo, Kyoko; Lloyd, Karen G.; F. Biddle, Jennifer The ISME Journal, Vol. 6, Issue 10 https://doi.org/10.1038/ismej.2012.37	journal	May 2012
Crystal Structure of Methyl-Coenzyme M Reductase: The Key Enzyme of Biological Methane Formation Ermler, U. Science, Vol. 278, Issue 5342 https://doi.org/10.1126/science.278.5342.1457	journal	November 1997
A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea Arshad, Arslan; Speth, Daan R.; de Graaf, Rob M. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01423	journal	December 2015
Anaerobic Oxidation of Methane: Progress with an Unknown Process Knittel, Katrin; Boetius, Antje Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093130	journal	October 2009
Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group Meyerdierks, Anke; Kube, Michael; Kostadinov, Ivaylo Environmental Microbiology, Vol. 12, Issue 2 https://doi.org/10.1111/j.1462-2920.2009.02083.x	journal	February 2010
Extreme Deviations from Expected Evolutionary Rates in Archaeal Protein Families Petitjean, Celine; Makarova, Kira S.; Wolf, Yuri I. Genome Biology and Evolution, Vol. 9, Issue 10 https://doi.org/10.1093/gbe/evx189	journal	September 2017
Novel reactions involved in energy conservation by methanogenic archaea Deppenmeier, Uwe; Lienard, Tanja; Gottschalk, Gerhard FEBS Letters, Vol. 457, Issue 3 https://doi.org/10.1016/S0014-5793(99)01026-1	journal	September 1999
Coupling of ferredoxin and heterodisulfide reduction via electron bifurcation in hydrogenotrophic methanogenic archaea Kaster, A. -K.; Moll, J.; Parey, K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 7 https://doi.org/10.1073/pnas.1016761108	journal	January 2011
Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor Girguis, P. R.; Orphan, V. J.; Hallam, S. J. Applied and Environmental Microbiology, Vol. 69, Issue 9 https://doi.org/10.1128/AEM.69.9.5472-5482.2003	journal	September 2003
Methanosaeta harundinacea sp. nov., a novel acetate-scavenging methanogen isolated from a UASB reactor Ma, K. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 1 https://doi.org/10.1099/ijs.0.63887-0	journal	January 2006
Evidence for the involvement of two heterodisulfide reductases in the energy-conserving system of Methanomassiliicoccus luminyensis Kröninger, Lena; Berger, Stefanie; Welte, Cornelia FEBS Journal, Vol. 283, Issue 3 https://doi.org/10.1111/febs.13594	journal	December 2015
Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. Sprenger, W. W.; van Belzen, M. C.; Rosenberg, J. International Journal of Systematic and Evolutionary Microbiology, Vol. 50, Issue 6 https://doi.org/10.1099/00207713-50-6-1989	journal	November 2000
A marine microbial consortium apparently mediating anaerobic oxidation of methane Boetius, Antje; Ravenschlag, Katrin; Schubert, Carsten J. Nature, Vol. 407, Issue 6804 https://doi.org/10.1038/35036572	journal	October 2000
Higher-level classification of the Archaea: evolution of methanogenesis and methanogens Bapteste, Éric; Brochier, Céline; Boucher, Yan Archaea, Vol. 1, Issue 5 https://doi.org/10.1155/2005/859728	journal	January 2005
Thermophilic archaea activate butane via alkyl-coenzyme M formation Laso-Pérez, Rafael; Wegener, Gunter; Knittel, Katrin Nature, Vol. 539, Issue 7629 https://doi.org/10.1038/nature20152	journal	October 2016
Oceanic Methane Biogeochemistry Reeburgh, William S. Chemical Reviews, Vol. 107, Issue 2 https://doi.org/10.1021/cr050362v	journal	February 2007
Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics Evans, P. N.; Parks, D. H.; Chadwick, G. L. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac7745	journal	October 2015
Ecological Aspects of the Distribution of Different Autotrophic CO ₂ Fixation Pathways Berg, Ivan A. Applied and Environmental Microbiology, Vol. 77, Issue 6 https://doi.org/10.1128/AEM.02473-10	journal	January 2011
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage Haroon, Mohamed F.; Hu, Shihu; Shi, Ying Nature, Vol. 500, Issue 7464 https://doi.org/10.1038/nature12375	journal	July 2013
Energy Metabolism during Anaerobic Methane Oxidation in ANME Archaea McGlynn, Shawn E. Microbes and environments, Vol. 32, Issue 1 https://doi.org/10.1264/jsme2.ME16166	journal	January 2017
Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life Spang, Anja; Caceres, Eva F.; Ettema, Thijs J. G. Science, Vol. 357, Issue 6351 https://doi.org/10.1126/science.aaf3883	journal	August 2017
Metabolic traits of an uncultured archaeal lineage -MSBL1- from brine pools of the Red Sea Mwirichia, Romano; Alam, Intikhab; Rashid, Mamoon Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19181	journal	January 2016
Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments: Genomic content of uncultured benthic Bathyarchaeota Lazar, Cassandre Sara; Baker, Brett J.; Seitz, Kiley Environmental Microbiology, Vol. 18, Issue 4 https://doi.org/10.1111/1462-2920.13142	journal	January 2016
Prokaryotic Populations and Activities in an Interbedded Coal Deposit, Including a Previously Deeply Buried Section (1.6–2.3 km) Above ∼ 150 Ma Basement Rock Fry, John C.; Horsfield, Brian; Sykes, Richard Geomicrobiology Journal, Vol. 26, Issue 3 https://doi.org/10.1080/01490450902724832	journal	March 2009
Lokiarchaeon is hydrogen dependent Sousa, Filipa L.; Neukirchen, Sinje; Allen, John F. Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.34	journal	April 2016
ATP synthases from archaea: The beauty of a molecular motor Grüber, Gerhard; Manimekalai, Malathy Sony Subramanian; Mayer, Florian Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 6 https://doi.org/10.1016/j.bbabio.2014.03.004	journal	June 2014
Methane production from coal by a single methanogen Mayumi, D.; Mochimaru, H.; Tamaki, H. Science, Vol. 354, Issue 6309 https://doi.org/10.1126/science.aaf8821	journal	October 2016
The Na+-translocating methyltransferase complex from methanogenic archaea Gottschalk, Gerhard; Thauer, Rudolf K. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1505, Issue 1 https://doi.org/10.1016/S0005-2728(00)00274-7	journal	May 2001
Three decades of global methane sources and sinks Kirschke, Stefanie; Bousquet, Philippe; Ciais, Philippe Nature Geoscience, Vol. 6, Issue 10 https://doi.org/10.1038/ngeo1955	journal	September 2013
Integrative modeling of gene and genome evolution roots the archaeal tree of life Williams, Tom A.; Szöllősi, Gergely J.; Spang, Anja Proceedings of the National Academy of Sciences, Vol. 114, Issue 23 https://doi.org/10.1073/pnas.1618463114	journal	May 2017
Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria Wegener, Gunter; Krukenberg, Viola; Riedel, Dietmar Nature, Vol. 526, Issue 7574 https://doi.org/10.1038/nature15733	journal	October 2015
The primary divisions of life: a phylogenomic approach employing composition-heterogeneous methods Foster, Peter G.; Cox, Cymon J.; Embley, T. Martin Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 364, Issue 1527 https://doi.org/10.1098/rstb.2009.0034	journal	August 2009
Phylogenetically Driven Sequencing of Extremely Halophilic Archaea Reveals Strategies for Static and Dynamic Osmo-response Becker, Erin A.; Seitzer, Phillip M.; Tritt, Andrew PLoS Genetics, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pgen.1004784	journal	November 2014
Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments Dombrowski, Nina; Seitz, Kiley W.; Teske, Andreas P. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0322-2	journal	August 2017
The growing tree of Archaea: new perspectives on their diversity, evolution and ecology Adam, Panagiotis S.; Borrel, Guillaume; Brochier-Armanet, Céline The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.122	journal	August 2017
Horizontal gene transfer constrains the timing of methanogen evolution Wolfe, Joanna M.; Fournier, Gregory P. Nature Ecology & Evolution, Vol. 2, Issue 5 https://doi.org/10.1038/s41559-018-0513-7	journal	April 2018
The two-domain tree of life is linked to a new root for the Archaea Raymann, Kasie; Brochier-Armanet, Céline; Gribaldo, Simonetta Proceedings of the National Academy of Sciences, Vol. 112, Issue 21 https://doi.org/10.1073/pnas.1420858112	journal	May 2015
Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen Nobu, Masaru Konishi; Narihiro, Takashi; Kuroda, Kyohei The ISME Journal, Vol. 10, Issue 10 https://doi.org/10.1038/ismej.2016.33	journal	March 2016
Environmental controls on intragroup diversity of the uncultured benthic archaea of the miscellaneous Crenarchaeotal group lineage naturally enriched in anoxic sediments of the White Oak River estuary (North Carolina, USA) : MCG intragroup diversity in estuary sediments Lazar, Cassandre Sara; Biddle, Jennifer F.; Meador, Travis B. Environmental Microbiology, Vol. 17, Issue 7 https://doi.org/10.1111/1462-2920.12659	journal	January 2015
Isolation of a novel acidiphilic methanogen from an acidic peat bog Bräuer, Suzanna L.; Cadillo-Quiroz, Hinsby; Yashiro, Erika Nature, Vol. 442, Issue 7099 https://doi.org/10.1038/nature04810	journal	May 2006
Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments Orphan, V. J.; House, C. H.; Hinrichs, K.-U. Proceedings of the National Academy of Sciences, Vol. 99, Issue 11, p. 7663-7668 https://doi.org/10.1073/pnas.072210299	journal	May 2002
Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis Lie, T. J.; Costa, K. C.; Lupa, B. Proceedings of the National Academy of Sciences, Vol. 109, Issue 38 https://doi.org/10.1073/pnas.1208779109	journal	August 2012
Gene transfers can date the tree of life Davín, Adrián A.; Tannier, Eric; Williams, Tom A. Nature Ecology & Evolution, Vol. 2, Issue 5 https://doi.org/10.1038/s41559-018-0525-3	journal	April 2018
Phylogenetic and Structural Comparisons of the Three Types of Methyl Coenzyme M Reductase from Methanococcales and Methanobacteriales Wagner, Tristan; Wegner, Carl-Eric; Kahnt, Jörg Journal of Bacteriology, Vol. 199, Issue 16 https://doi.org/10.1128/JB.00197-17	journal	May 2017
Isolation of Key Methanogens for Global Methane Emission from Rice Paddy Fields: a Novel Isolate Affiliated with the Clone Cluster Rice Cluster I Sakai, Sanae; Imachi, Hiroyuki; Sekiguchi, Yuji Applied and Environmental Microbiology, Vol. 73, Issue 13 https://doi.org/10.1128/AEM.03008-06	journal	May 2007
Biochemistry of methanogenesis: a tribute to Marjory Stephenson:1998 Marjory Stephenson Prize Lecture Thauer, R. K. Microbiology, Vol. 144, Issue 9 https://doi.org/10.1099/00221287-144-9-2377	journal	September 1998
Methane from acetate. Ferry, J. G. Journal of Bacteriology, Vol. 174, Issue 17 https://doi.org/10.1128/jb.174.17.5489-5495.1992	journal	September 1992
Methanogenic archaea database containing physiological and biochemical characteristics Łukaszewicz, Marcin; Jabłoński, Sławomir; Rodowicz, Paweł International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue 4 https://doi.org/10.1099/ijs.0.000065	journal	April 2015
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L. Science, Vol. 354, Issue 6310 https://doi.org/10.1126/science.aag2947	journal	October 2016
Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction Seitz, Kiley W.; Lazar, Cassandre S.; Hinrichs, Kai-Uwe The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.233	journal	January 2016
Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics Hallam, S. J. Science, Vol. 305, Issue 5689 https://doi.org/10.1126/science.1100025	journal	September 2004
Reverse Methanogenesis and Respiration in Methanotrophic Archaea Timmers, Peer H. A.; Welte, Cornelia U.; Koehorst, Jasper J. Archaea, Vol. 2017 https://doi.org/10.1155/2017/1654237	journal	January 2017
The Anaerobic Oxidation of Methane: New Insights in Microbial Ecology and Biogeochemistry Hinrichs, K. -U.; Boetius, A. Ocean Margin Systems https://doi.org/10.1007/978-3-662-05127-6_28	book	January 2002
Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation Sieber, Jessica R.; McInerney, Michael J.; Gunsalus, Robert P. Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-090110-102844	journal	October 2012
Isolation and Characterization of a Thermophilic, Obligately Anaerobic and Heterotrophic Marine Chloroflexi Bacterium from a Chloroflexi-dominated Microbial Community Associated with a Japanese Shallow Hydrothermal System, and Proposal for Thermomarinilinea lacunofontalis gen. nov., sp. nov. Nunoura, Takuro; Hirai, Miho; Miyazaki, Masayuki Microbes and Environments, Vol. 28, Issue 2 https://doi.org/10.1264/jsme2.ME12193	journal	January 2013
The Genome Sequence of Methanosphaera stadtmanae Reveals Why This Human Intestinal Archaeon Is Restricted to Methanol and H2 for Methane Formation and ATP Synthesis Fricke, W. F.; Seedorf, H.; Henne, A. Journal of Bacteriology, Vol. 188, Issue 2 https://doi.org/10.1128/JB.188.2.642-658.2006	journal	December 2005
The Stepwise Evolution of Early Life Driven by Energy Conservation Ferry, J. G. Molecular Biology and Evolution, Vol. 23, Issue 6 https://doi.org/10.1093/molbev/msk014	journal	March 2006
Phenotypic characterization of Rice Cluster III archaea without prior isolation by applying quantitative polymerase chain reaction to an enrichment culture Kemnitz, Dana; Kolb, Steffen; Conrad, Ralf Environmental Microbiology, Vol. 7, Issue 4 https://doi.org/10.1111/j.1462-2920.2005.00723.x	journal	April 2005
The deep, hot biosphere: Twenty-five years of retrospection Colman, Daniel R.; Poudel, Saroj; Stamps, Blake W. Proceedings of the National Academy of Sciences, Vol. 114, Issue 27 https://doi.org/10.1073/pnas.1701266114	journal	July 2017
Discovery of a novel methanogen prevalent in thawing permafrost Mondav, Rhiannon; Woodcroft, Ben J.; Kim, Eun-Hae Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4212	journal	February 2014
Elucidation of the biosynthesis of the methane catalyst coenzyme F430 Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21427	journal	February 2017
The origin and evolution of Archaea: a state of the art Gribaldo, Simonetta; Brochier-Armanet, Celine Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1470 https://doi.org/10.1098/rstb.2006.1841	journal	May 2006
Marine microbes rapidly adapt to consume ethane, propane, and butane within the dissolved hydrocarbon plume of a natural seep Mendes, Stephanie D.; Redmond, Molly C.; Voigritter, Karl Journal of Geophysical Research: Oceans, Vol. 120, Issue 3 https://doi.org/10.1002/2014JC010362	journal	March 2015
Differences down-under: alcohol-fueled methanogenesis by archaea present in Australian macropodids Hoedt, Emily C.; Cuív, Páraic Ó; Evans, Paul N. The ISME Journal, Vol. 10, Issue 10 https://doi.org/10.1038/ismej.2016.41	journal	March 2016
The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus Klenk, Hans-Peter; Clayton, Rebecca A.; Tomb, Jean-Francois Nature, Vol. 390, Issue 6658 https://doi.org/10.1038/37052	journal	November 1997
Phylogenetic Comparison of the Methanogenic Communities from an Acidic, Oligotrophic Fen and an Anaerobic Digester Treating Municipal Wastewater Sludge Steinberg, L. M.; Regan, J. M. Applied and Environmental Microbiology, Vol. 74, Issue 21 https://doi.org/10.1128/AEM.00553-08	journal	September 2008
Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes Adam, Panagiotis S.; Borrel, Guillaume; Gribaldo, Simonetta Proceedings of the National Academy of Sciences, Vol. 115, Issue 6 https://doi.org/10.1073/pnas.1716667115	journal	January 2018
Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass Ferry, James G. Current Opinion in Biotechnology, Vol. 22, Issue 3 https://doi.org/10.1016/j.copbio.2011.04.011	journal	June 2011
Microbial community characteristics of petroleum reservoir production water amended with n-alkanes and incubated under nitrate-, sulfate-reducing and methanogenic conditions Li, Wei; Wang, Li-Ying; Duan, Ruo-Yu International Biodeterioration & Biodegradation, Vol. 69 https://doi.org/10.1016/j.ibiod.2012.01.005	journal	April 2012
Discovery of extremely halophilic, methyl-reducing euryarchaea provides insights into the evolutionary origin of methanogenesis Sorokin, Dimitry Y.; Makarova, Kira S.; Abbas, Ben Nature Microbiology, Vol. 2, Issue 8 https://doi.org/10.1038/nmicrobiol.2017.81	journal	May 2017
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria Nature Microbiology, Vol. 2, Issue 11 https://doi.org/10.1038/s41564-017-0012-7	journal	September 2017
Characterization of C1-Metabolizing Prokaryotic Communities in Methane Seep Habitats at the Kuroshima Knoll, Southern Ryukyu Arc, by Analyzing pmoA, mmoX, mxaF, mcrA, and 16S rRNA Genes Inagaki, F.; Tsunogai, U.; Suzuki, M. Applied and Environmental Microbiology, Vol. 70, Issue 12 https://doi.org/10.1128/AEM.70.12.7445-7455.2004	journal	December 2004
Novel Cultivation-Based Approach To Understanding the Miscellaneous Crenarchaeotic Group (MCG) Archaea from Sedimentary Ecosystems Gagen, Emma J.; Huber, Harald; Meador, Travis Applied and Environmental Microbiology, Vol. 79, Issue 20 https://doi.org/10.1128/AEM.02153-13	journal	August 2013
Methanogens: biochemical background and biotechnological applications Enzmann, Franziska; Mayer, Florian; Rother, Michael AMB Express, Vol. 8, Issue 1 https://doi.org/10.1186/s13568-017-0531-x	journal	January 2018
Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction Holler, T.; Wegener, G.; Niemann, H. Proceedings of the National Academy of Sciences, Vol. 108, Issue 52 https://doi.org/10.1073/pnas.1106032108	journal	December 2011
Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO2 Thauer, Rudolf K. Current Opinion in Microbiology, Vol. 14, Issue 3 https://doi.org/10.1016/j.mib.2011.03.003	journal	June 2011
Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea Baker, Brett J.; Saw, Jimmy H.; Lind, Anders E. Nature Microbiology, Vol. 1, Issue 3 https://doi.org/10.1038/nmicrobiol.2016.2	journal	February 2016
GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes Boyd, Joel A.; Woodcroft, Ben J.; Tyson, Gene W. Nucleic Acids Research, Vol. 46, Issue 10 https://doi.org/10.1093/nar/gky174	journal	March 2018
Unique Characteristics of the Pyrrolysine System in the 7th Order of Methanogens: Implications for the Evolution of a Genetic Code Expansion Cassette Borrel, Guillaume; Gaci, Nadia; Peyret, Pierre Archaea, Vol. 2014, p. 1-11 https://doi.org/10.1155/2014/374146	journal	January 2014
Enzymology of the Wood-Ljungdahl Pathway of Acetogenesis Ragsdale, Stephen W. Annals of the New York Academy of Sciences, Vol. 1125, Issue 1 https://doi.org/10.1196/annals.1419.015	journal	March 2008
Isolation and Characterization of Methanohalophilus portucalensis sp. nov. and DNA Reassociation Study of the Genus Methanohalophilus Boone, D. R.; Mathrani, I. M.; Liu, Y. International Journal of Systematic Bacteriology, Vol. 43, Issue 3 https://doi.org/10.1099/00207713-43-3-430	journal	July 1993
Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes Kelly, S.; Wickstead, B.; Gull, K. Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1708 https://doi.org/10.1098/rspb.2010.1427	journal	September 2010
On the origin of biochemistry at an alkaline hydrothermal vent Martin, William; Russell, Michael J. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 362, Issue 1486 https://doi.org/10.1098/rstb.2006.1881	journal	November 2006
The radical mechanism of biological methane synthesis by methyl-coenzyme M reductase Wongnate, T.; Sliwa, D.; Ginovska, B. Science, Vol. 352, Issue 6288 https://doi.org/10.1126/science.aaf0616	journal	May 2016
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota Vanwonterghem, Inka; Evans, Paul N.; Parks, Donovan H. Nature Microbiology, Vol. 1, Issue 12 https://doi.org/10.1038/nmicrobiol.2016.170	journal	October 2016
Archaea catalyze iron-dependent anaerobic oxidation of methane Ettwig, Katharina F.; Zhu, Baoli; Speth, Daan Proceedings of the National Academy of Sciences, Vol. 113, Issue 45 https://doi.org/10.1073/pnas.1609534113	journal	October 2016
The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill b Luton, Philip E.; Wayne, Jonathan M.; Sharp, Richard J. Microbiology, Vol. 148, Issue 11 https://doi.org/10.1099/00221287-148-11-3521	journal	November 2002
Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments He, Y.; Li, M.; Perumal, V. Nature Microbiology, Vol. 1, Issue 6 https://doi.org/10.1038/nmicrobiol.2016.35	journal	April 2016
Clusters of orthologous genes for 41 archaeal genomes and implications for evolutionary genomics of archaea Makarova, Kira S.; Sorokin, Alexander V.; Novichkov, Pavel S. Biology Direct, Vol. 2, Issue 1 https://doi.org/10.1186/1745-6150-2-33	journal	January 2007
Gene Acquisitions from Bacteria at the Origins of Major Archaeal Clades Are Vastly Overestimated Groussin, Mathieu; Boussau, Bastien; Szöllõsi, Gergely Molecular Biology and Evolution, Vol. 33, Issue 2 https://doi.org/10.1093/molbev/msv249	journal	November 2015
The Impact of Aridification and Vegetation Type on Changes in the Community Structure of Methane-Cycling Microorganisms in Japanese Wetland Soils Narihiro, Takashi; Hori, Tomoyuki; Nagata, Osamu Bioscience, Biotechnology, and Biochemistry, Vol. 75, Issue 9 https://doi.org/10.1271/bbb.110265	journal	September 2011
Early bioenergetic evolution Sousa, Filipa L.; Thiergart, Thorsten; Landan, Giddy Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1622 https://doi.org/10.1098/rstb.2013.0088	journal	July 2013
Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways Wang, Feng-Ping; Zhang, Yu; Chen, Ying The ISME Journal, Vol. 8, Issue 5 https://doi.org/10.1038/ismej.2013.212	journal	December 2013
Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens Welte, Cornelia; Deppenmeier, Uwe Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7 https://doi.org/10.1016/j.bbabio.2013.12.002	journal	July 2014
Diversity and Abundance of Aerobic and Anaerobic Methane Oxidizers at the Haakon Mosby Mud Volcano, Barents Sea Losekann, T.; Knittel, K.; Nadalig, T. Applied and Environmental Microbiology, Vol. 73, Issue 10 https://doi.org/10.1128/AEM.00016-07	journal	March 2007
Mutagenesis of the C1 Oxidation Pathway in Methanosarcina barkeri: New Insights into the Mtr/Mer Bypass Pathway Welander, P. V.; Metcalf, W. W. Journal of Bacteriology, Vol. 190, Issue 6 https://doi.org/10.1128/JB.01424-07	journal	January 2008
Methanogenesis and the Wood–Ljungdahl Pathway: An Ancient, Versatile, and Fragile Association Borrel, Guillaume; Adam, Panagiotis S.; Gribaldo, Simonetta Genome Biology and Evolution, Vol. 8, Issue 6 https://doi.org/10.1093/gbe/evw114	journal	May 2016

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