Methanotrophy across a natural permafrost thaw environment

Singleton, Caitlin M.; McCalley, Carmody K.; Woodcroft, Ben J.; Boyd, Joel A.; Evans, Paul N.; Hodgkins, Suzanne B.; Chanton, Jeffrey P.; Frolking, Steve; Crill, Patrick M.; Saleska, Scott R.; Rich, Virginia I.; Tyson, Gene W.

doi:10.1038/s41396-018-0065-5

Title: Methanotrophy across a natural permafrost thaw environment

Journal Article · 28 June 2018 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-018-0065-5 · OSTI ID:1481728

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Univ. of Queensland, Brisbane, QLD (Australia)
Rochester Institute of Technology, Rochester, NY (United States)
Florida State Univ., Tallahassee, FL (United States)
Univ. of New Hampshire, Durham, NH (United States)
Stockholm Univ., Stockholm (Sweden)
Univ. of Arizona, Tucson, AZ (United States)
The Ohio State Univ., Columbus, OH (United States)

The fate of carbon sequestered in permafrost is a key concern for future global warming as this large carbon stock is rapidly becoming a net methane source due to widespread thaw. Methane release from permafrost is moderated by methanotrophs, which oxidise 20-60% of this methane before emission to the atmosphere. Despite the importance of methanotrophs to carbon cycling, these microorganisms are under-characterised and have not been studied across a natural permafrost thaw gradient. Here, we examine methanotroph communities from the active layer of a permafrost thaw gradient in Stordalen Mire (Abisko, Sweden) spanning three years, analysing 188 metagenomes and 24 metatranscriptomes paired with in situ biogeochemical data. Methanotroph community composition and activity varied significantly as thaw progressed from intact permafrost palsa, to partially-thawed bog and fully-thawed fen. Thirteen methanotroph population genomes were recovered, including two novel genomes belonging to the uncultivated upland soil cluster alpha (USCα) group and a novel potentially methanotrophic Hyphomicrobiaceae. Combined analysis of porewater δ¹³C-CH₄ isotopes and methanotroph abundances showed methane oxidation was greatest below the oxic-anoxic interface in the bog. Here, these results detail the direct effect of thaw on autochthonous methanotroph communities, and their consequent changes in population structure, activity, and methane moderation potential.

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Research Organization:: Univ. of Queensland, Brisbane, QLD (Australia). Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences

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

Grant/Contract Number:: SC0016440

OSTI ID:: 1481728

Journal Information:: The ISME Journal, Vol. 12, Issue 10; Related Information: Raw DNA and RNA sequencing data:https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA386568; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 80 works

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References (135)

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
A novel family of functional operons encoding methane/ammonia monooxygenase-related proteins in gammaproteobacterial methanotrophs: Novel monooxygenase in Gamma-MOB Tavormina, Patricia L.; Orphan, Victoria J.; Kalyuzhnaya, Marina G. Environmental Microbiology Reports, Vol. 3, Issue 1 https://doi.org/10.1111/j.1758-2229.2010.00192.x	journal	February 2011
Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms Tveit, Alexander; Schwacke, Rainer; Svenning, Mette M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.99	journal	September 2012
One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic–anoxic interface in a flooded paddy soil Reim, Andreas; Lüke, Claudia; Krause, Sascha The ISME Journal, Vol. 6, Issue 11 https://doi.org/10.1038/ismej.2012.57	journal	June 2012
Genomic and Transcriptomic Analyses of the Facultative Methanotroph Methylocystis sp. Strain SB2 Grown on Methane or Ethanol Vorobev, Alexey; Jagadevan, Sheeja; Jain, Sunit Applied and Environmental Microbiology, Vol. 80, Issue 10 https://doi.org/10.1128/AEM.00218-14	journal	March 2014
Reconstructing terrestrial nutrient cycling using stable nitrogen isotopes in wood Gerhart, Laci M.; McLauchlan, Kendra K. Biogeochemistry, Vol. 120, Issue 1-3 https://doi.org/10.1007/s10533-014-9988-8	journal	May 2014
CH ₄ oxidation by tundra wetlands as measured by a selective inhibitor technique Moosavi, Sadredin C.; Crill, Patrick M. Journal of Geophysical Research: Atmospheres, Vol. 103, Issue D22 https://doi.org/10.1029/97JD03519	journal	November 1998
Genomic Reconstruction of an Uncultured Hydrothermal Vent Gammaproteobacterial Methanotroph (Family Methylothermaceae) Indicates Multiple Adaptations to Oxygen Limitation Skennerton, Connor T.; Ward, Lewis M.; Michel, Alice Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01425	journal	December 2015
Autotrophic Methanotrophy in Verrucomicrobia: Methylacidiphilum fumariolicumSolV Uses the Calvin-Benson-Bassham Cycle for Carbon Dioxide Fixation Khadem, A. F.; Pol, A.; Wieczorek, A. Journal of Bacteriology, Vol. 193, Issue 17 https://doi.org/10.1128/JB.00407-11	journal	July 2011
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/MMBR.60.2.439-471.1996	journal	January 1996
Genome-guided insight into the methylotrophy of Paracoccus aminophilus JCM 7686 Dziewit, Lukasz; Czarnecki, Jakub; Prochwicz, Emilia Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00852	journal	August 2015
Methane-cycling communities in a permafrost-affected soil on Herschel Island, Western Canadian Arctic: active layer profiling of mcrA and pmoA genes Barbier, Béatrice A.; Dziduch, Isabel; Liebner, Susanne FEMS Microbiology Ecology, Vol. 82, Issue 2 https://doi.org/10.1111/j.1574-6941.2012.01332.x	journal	March 2012
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center Anantharaman, Karthik; Breier, John A.; Dick, Gregory J. The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.81	journal	June 2015
A scalable model for methane consumption in arctic mineral soils Oh, Youmi; Stackhouse, Brandon; Lau, Maggie C. Y. Geophysical Research Letters, Vol. 43, Issue 10 https://doi.org/10.1002/2016GL069049	journal	May 2016
Modularity of methylotrophy, revisited: Modularity of methylotrophy, revisited Chistoserdova, Ludmila Environmental Microbiology, Vol. 13, Issue 10 https://doi.org/10.1111/j.1462-2920.2011.02464.x	journal	March 2011
An active atmospheric methane sink in high Arctic mineral cryosols Lau, M. C. Y.; Stackhouse, B. T.; Layton, A. C. The ISME Journal, Vol. 9, Issue 8 https://doi.org/10.1038/ismej.2015.13	journal	April 2015
Molecular characterization of structural genes coding for a membrane bound hydrogenase in Methylococcus capsulatus (Bath) CsÃ¡ki, R.; HanczÃ¡r, T.; Bodrossy, L. FEMS Microbiology Letters, Vol. 205, Issue 2 https://doi.org/10.1111/j.1574-6968.2001.tb10948.x	journal	December 2001
Draft Genome Sequence of Methyloferula stellata AR4, an Obligate Methanotroph Possessing Only a Soluble Methane Monooxygenase Dedysh, Svetlana N.; Naumoff, Daniil G.; Vorobev, Alexey V. Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomeA.01555-14	journal	March 2015
Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions: Methane, microbes and models Nazaries, Loïc; Murrell, J. Colin; Millard, Pete Environmental Microbiology, Vol. 15, Issue 9 https://doi.org/10.1111/1462-2920.12149	journal	May 2013
Diverse electron sources support denitrification under hypoxia in the obligate methanotroph Methylomicrobium album strain BG8 Kits, K. Dimitri; Campbell, Dustin J.; Rosana, Albert R. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01072	journal	October 2015
Poly-3-Hydroxybutyrate Metabolism in the Type II Methanotroph Methylocystis parvus OBBP Pieja, Allison J.; Sundstrom, Eric R.; Criddle, Craig S. Applied and Environmental Microbiology, Vol. 77, Issue 17, p. 6012-6019 https://doi.org/10.1128/aem.00509-11	journal	July 2011
Distribution, diversity and ecology of aerobic CO-oxidizing bacteria King, Gary M.; Weber, Carolyn F. Nature Reviews Microbiology, Vol. 5, Issue 2 https://doi.org/10.1038/nrmicro1595	journal	February 2007
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences Luo, Chengwei; Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. Nucleic Acids Research, Vol. 42, Issue 8 https://doi.org/10.1093/nar/gku169	journal	March 2014
Revisiting life strategy concepts in environmental microbial ecology Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fix006	journal	January 2017
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker Knief, Claudia Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01346	journal	December 2015
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Commensal Pseudomonas protect Arabidopsis thaliana from a coexisting pathogen via multiple lineage-dependent mechanisms Shalev, Or; Ashkenazy, Haim; Neumann, Manuela The ISME Journal, Vol. 16, Issue 5 https://doi.org/10.1038/s41396-021-01168-6	journal	December 2021
The (d)evolution of methanotrophy in the Beijerinckiaceae—a comparative genomics analysis Tamas, Ivica; Smirnova, Angela V.; He, Zhiguo The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.145	journal	August 2013
Genome-centric view of carbon processing in thawing permafrost Woodcroft, Ben J.; Singleton, Caitlin M.; Boyd, Joel A. Nature, Vol. 560, Issue 7716 https://doi.org/10.1038/s41586-018-0338-1	journal	July 2018
Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia Dunfield, Peter F.; Yuryev, Anton; Senin, Pavel Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06411	journal	November 2007
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
Three decades of global methane sources and sinks Ciais, Philippe; Kummel, Paul B.; Zeng, Guang Nature Publishing Group https://doi.org/10.7892/boris.47715	text	January 2013
Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia Dunfield, Peter F.; Yuryev, Anton; Senin, Pavel Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06411	journal	November 2007
Methylacidiphilum fumariolicum SolV, a thermoacidophilic ‘Knallgas’ methanotroph with both an oxygen-sensitive and -insensitive hydrogenase Mohammadi, Sepehr; Pol, Arjan; van Alen, Theo A. The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2016.171	journal	December 2016
New Proteins Involved in Sulfur Trafficking in the Cytoplasm of Allochromatium vinosum Stockdreher, Yvonne; Sturm, Marga; Josten, Michaele Journal of Biological Chemistry, Vol. 289, Issue 18 https://doi.org/10.1074/jbc.m113.536425	journal	March 2014
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts611	journal	October 2012
Diversity of Aerobic Methanotrophic Bacteria in a Permafrost Active Layer Soil of the Lena Delta, Siberia Liebner, Susanne; Rublack, Katja; Stuehrmann, Torben Microbial Ecology, Vol. 57, Issue 1 https://doi.org/10.1007/s00248-008-9411-x	journal	July 2008
Methylacidiphilum fumariolicum SolV, a thermoacidophilic ‘Knallgas’ methanotroph with both an oxygen-sensitive and -insensitive hydrogenase Mohammadi, Sepehr; Pol, Arjan; van Alen, Theo A. The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2016.171	journal	December 2016
HydDB: A web tool for hydrogenase classification and analysis Søndergaard, Dan; Pedersen, Christian N. S.; Greening, Chris Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34212	journal	September 2016
Assimilation of acetate by the putative atmospheric methane oxidizers belonging to the USCα clade: Acetate assimilation by USCα Pratscher, Jennifer; Dumont, Marc G.; Conrad, Ralf Environmental Microbiology, Vol. 13, Issue 10 https://doi.org/10.1111/j.1462-2920.2011.02537.x	journal	August 2011
Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions Krause, Sascha M. B.; Johnson, Timothy; Samadhi Karunaratne, Yasodara Proceedings of the National Academy of Sciences, Vol. 114, Issue 2 https://doi.org/10.1073/pnas.1619871114	journal	December 2016
Methylohalobius crimeensis gen. nov., sp. nov., a moderately halophilic, methanotrophic bacterium isolated from hypersaline lakes of Crimea Heyer, J. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 5 https://doi.org/10.1099/ijs.0.63213-0	journal	September 2005
Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2 Baani, M.; Liesack, W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 29 https://doi.org/10.1073/pnas.0702643105	journal	July 2008
Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea Ghosh, Wriddhiman; Dam, Bomba FEMS Microbiology Reviews, Vol. 33, Issue 6 https://doi.org/10.1111/j.1574-6976.2009.00187.x	journal	November 2009
Sulfate-reducing microorganisms in wetlands – fameless actors in carbon cycling and climate change Pester, Michael Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00072	journal	January 2012
Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions Krause, Sascha M. B.; Johnson, Timothy; Samadhi Karunaratne, Yasodara Proceedings of the National Academy of Sciences, Vol. 114, Issue 2 https://doi.org/10.1073/pnas.1619871114	journal	December 2016
Nitrite-driven anaerobic methane oxidation by oxygenic bacteria Ettwig, Katharina F.; Butler, Margaret K.; Le Paslier, Denis Nature, Vol. 464, Issue 7288 https://doi.org/10.1038/nature08883	journal	March 2010
The quest for atmospheric methane oxidizers in forest soils: Atmospheric methane-oxidizing methanotrophs in forest soils Kolb, Steffen Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00047.x	journal	July 2009
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Methanotrophy below pH 1 by a new Verrucomicrobia species Pol, Arjan; Heijmans, Klaas; Harhangi, Harry R. Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06222	journal	November 2007
Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 16 https://doi.org/10.1073/pnas.1314641111	journal	April 2014
PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim Applied Microbiology and Biotechnology, Vol. 98, Issue 14 https://doi.org/10.1007/s00253-014-5766-8	journal	May 2014
Methane dynamics regulated by microbial community response to permafrost thaw McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B. Nature, Vol. 514, Issue 7523 https://doi.org/10.1038/nature13798	journal	October 2014
Methyloferula stellata gen. nov., sp. nov., an acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase Vorobev, A. V.; Baani, M.; Doronina, N. V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 10 https://doi.org/10.1099/ijs.0.028118-0	journal	November 2010
Formaldehyde Stress Responses in Bacterial Pathogens Chen, Nathan H.; Djoko, Karrera Y.; Veyrier, Frédéric J. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00257	journal	March 2016
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
Anaerobic oxidation of methane in tropical and boreal soils: Ecological significance in terrestrial methane cycling: ANAEROBIC OXIDATION OF METHANE IN SOILS Blazewicz, Steven J.; Petersen, Dorthe G.; Waldrop, Mark P. Journal of Geophysical Research: Biogeosciences, Vol. 117, Issue G2 https://doi.org/10.1029/2011JG001864	journal	June 2012
Model of the molecular basis for hydroxylamine oxidation and nitrous oxide production in methanotrophic bacteria: N-metabolism gene inventory in methanotrophic bacteria Campbell, Mark A.; Nyerges, Györgyi; Kozlowski, Jessica A. FEMS Microbiology Letters, Vol. 322, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02340.x	journal	July 2011
Ancient Permafrost and a Future, Warmer Arctic Froese, D. G.; Westgate, J. A.; Reyes, A. V. Science, Vol. 321, Issue 5896 https://doi.org/10.1126/science.1157525	journal	September 2008
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
IMG ER: a system for microbial genome annotation expert review and curation Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N. Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp393	journal	June 2009
Distribution, diversity and ecology of aerobic CO-oxidizing bacteria King, Gary M.; Weber, Carolyn F. Nature Reviews Microbiology, Vol. 5, Issue 2 https://doi.org/10.1038/nrmicro1595	journal	February 2007
Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1420797112	journal	April 2015
Reviews and syntheses: Four decades of modeling methane cycling in terrestrial ecosystems Xu, Xiaofeng; Yuan, Fengming; Hanson, Paul J. Biogeosciences, Vol. 13, Issue 12 https://doi.org/10.5194/bg-13-3735-2016	journal	January 2016
Diverse electron sources support denitrification under hypoxia in the obligate methanotroph Methylomicrobium album strain BG8 Kits, K. Dimitri; Campbell, Dustin J.; Rosana, Albert R. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01072	journal	October 2015
Soil organic carbon pools in the northern circumpolar permafrost region: SOIL ORGANIC CARBON POOLS Tarnocai, C.; Canadell, J. G.; Schuur, E. A. G. Global Biogeochemical Cycles, Vol. 23, Issue 2 https://doi.org/10.1029/2008GB003327	journal	June 2009
Methane, microbes and models: fundamental understanding of the soil methane cycle for future predictions: Methane, microbes and models Nazaries, Loïc; Murrell, J. Colin; Millard, Pete Environmental Microbiology, Vol. 15, Issue 9 https://doi.org/10.1111/1462-2920.12149	journal	May 2013
Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships Tabita, F. R.; Satagopan, S.; Hanson, T. E. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/erm361	journal	June 2007
Metatranscriptomic Analysis of Arctic Peat Soil Microbiota Tveit, Alexander T.; Urich, Tim; Svenning, Mette M. Applied and Environmental Microbiology, Vol. 80, Issue 18 https://doi.org/10.1128/AEM.01030-14	journal	July 2014
Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms Tveit, Alexander; Schwacke, Rainer; Svenning, Mette M. The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.99	journal	September 2012
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
Methanotrophic and Methanogenic Communities in Swiss Alpine Fens Dominated by Carex rostrata and Eriophorum angustifolium Cheema, Simrita; Zeyer, Josef; Henneberger, Ruth Applied and Environmental Microbiology, Vol. 81, Issue 17 https://doi.org/10.1128/AEM.01519-15	journal	June 2015
XoxF Acts as the Predominant Methanol Dehydrogenase in the Type I Methanotroph Methylomicrobium buryatense Chu, Frances; Lidstrom, Mary E. Journal of Bacteriology, Vol. 198, Issue 8 https://doi.org/10.1128/JB.00959-15	journal	February 2016
Isolation, sequencing, and mutagenesis of the gene encoding NAD- and glutathione-dependent formaldehyde dehydrogenase (GD-FALDH) from Paracoccus denitrificans, in which GD-FALDH is essential for methylotrophic growth. Ras, J.; Van Ophem, P. W.; Reijnders, W. N. Journal of Bacteriology, Vol. 177, Issue 1 https://doi.org/10.1128/jb.177.1.247-251.1995	journal	January 1995
Salinimonas marina sp. nov. Isolated from Jeju Island Marine Sediment Kim, Minji; Lee, Ki-Eun; Cha, In-Tae Current Microbiology, Vol. 78, Issue 8 https://doi.org/10.1007/s00284-021-02576-9	journal	June 2021
Climate change and the permafrost carbon feedback Schuur, E. A. G.; McGuire, A. D.; Schädel, C. Nature, Vol. 520, Issue 7546 https://doi.org/10.1038/nature14338	journal	April 2015
Draft Genome Sequence of Comamonas aquatilis Strain LK (= CSUR P6418 = CECT 9772), Isolated from the Planarian Schmidtea mediterranea Kangale, Luis Johnson; Levasseur, Anthony; Raoult, Didier Microbiology Resource Announcements, Vol. 10, Issue 5 https://doi.org/10.1128/mra.00297-20	journal	February 2021
First Genome Data from Uncultured Upland Soil Cluster Alpha Methanotrophs Provide Further Evidence for a Close Phylogenetic Relationship to Methylocapsa acidiphila B2 and for High-Affinity Methanotrophy Involving Particulate Methane Monooxygenase Ricke, P.; Kube, M.; Nakagawa, S. Applied and Environmental Microbiology, Vol. 71, Issue 11 https://doi.org/10.1128/AEM.71.11.7472-7482.2005	journal	November 2005
Modeling CH4 and CO2 cycling using porewater stable isotopes in a thermokarst bog in Interior Alaska: results from three conceptual reaction networks Neumann, Rebecca B.; Blazewicz, Steven J.; Conaway, Christopher H. Biogeochemistry, Vol. 127, Issue 1 https://doi.org/10.1007/s10533-015-0168-2	journal	December 2015
MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences Luo, Chengwei; Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. Nucleic Acids Research, Vol. 42, Issue 8 https://doi.org/10.1093/nar/gku169	journal	March 2014
Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival Greening, Chris; Biswas, Ambarish; Carere, Carlo R. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.153	journal	September 2015
An active atmospheric methane sink in high Arctic mineral cryosols Lau, M. C. Y.; Stackhouse, B. T.; Layton, A. C. The ISME Journal, Vol. 9, Issue 8 https://doi.org/10.1038/ismej.2015.13	journal	April 2015
Molecular characterization of structural genes coding for a membrane bound hydrogenase in Methylococcus capsulatus (Bath) CsÃ¡ki, R.; HanczÃ¡r, T.; Bodrossy, L. FEMS Microbiology Letters, Vol. 205, Issue 2 https://doi.org/10.1111/j.1574-6968.2001.tb10948.x	journal	December 2001
The (d)evolution of methanotrophy in the Beijerinckiaceae—a comparative genomics analysis Tamas, Ivica; Smirnova, Angela V.; He, Zhiguo The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.145	journal	August 2013
Facultative methanotrophy: false leads, true results, and suggestions for future research: Facultative methanotrophy Semrau, Jeremy D.; DiSpirito, Alan A.; Vuilleumier, Stéphane FEMS Microbiology Letters, Vol. 323, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02315.x	journal	June 2011
Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 16 https://doi.org/10.1073/pnas.1314641111	journal	April 2014
Massilia aromaticivorans sp. nov., a BTEX Degrading Bacterium Isolated from Arctic Soil Son, Jigwan; Lee, Hyosun; Kim, Mincheol Current Microbiology, Vol. 78, Issue 5 https://doi.org/10.1007/s00284-021-02379-y	journal	April 2021
Reviews and syntheses: Four decades of modeling methane cycling in terrestrial ecosystems Xu, Xiaofeng; Yuan, Fengming; Hanson, Paul J. Biogeosciences, Vol. 13, Issue 12 https://doi.org/10.5194/bg-13-3735-2016	journal	January 2016
IMG ER: a system for microbial genome annotation expert review and curation Markowitz, Victor M.; Mavromatis, Konstantinos; Ivanova, Natalia N. Bioinformatics, Vol. 25, Issue 17 https://doi.org/10.1093/bioinformatics/btp393	journal	June 2009
Seasonal patterns of methane uptake and carbon dioxide release by a temperate woodland soil Crill, Patrick M. Global Biogeochemical Cycles, Vol. 5, Issue 4 https://doi.org/10.1029/91GB02466	journal	December 1991
Characterization and functional analysis of phytoene synthase gene family in tobacco Wang, Zhaojun; Zhang, Lin; Dong, Chen BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-020-02816-3	journal	January 2021
Rhodomicrobium udaipurense sp. nov., a psychrotolerant, phototrophic alphaproteobacterium isolated from a freshwater stream Ramana, V. V.; Raj, P. S.; Tushar, L. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 7 https://doi.org/10.1099/ijs.0.046409-0	journal	January 2013
Methyloferula stellata gen. nov., sp. nov., an acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase Vorobev, A. V.; Baani, M.; Doronina, N. V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 10 https://doi.org/10.1099/ijs.0.028118-0	journal	November 2010
Heterologous expression of heterotrophic nitrification genes Crossman, L. C.; Moir, J. W. B.; Enticknap, J. J. Microbiology, Vol. 143, Issue 12 https://doi.org/10.1099/00221287-143-12-3775	journal	December 1997
Evaluation of methane oxidation in therhizosphere of a Carex dominated fen in northcentral Alberta, Canada Popp, Trevor J.; Chanton, Jeffrey P.; Whiting, Gary J. Biogeochemistry, Vol. 51, Issue 3, p. 259-281 https://doi.org/10.1023/A:1006452609284	journal	January 2000
PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim Applied Microbiology and Biotechnology, Vol. 98, Issue 14 https://doi.org/10.1007/s00253-014-5766-8	journal	May 2014
Genomic Reconstruction of an Uncultured Hydrothermal Vent Gammaproteobacterial Methanotroph (Family Methylothermaceae) Indicates Multiple Adaptations to Oxygen Limitation Skennerton, Connor T.; Ward, Lewis M.; Michel, Alice Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01425	journal	December 2015
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
Identification and characterization of multiple rubisco activases in chemoautotrophic bacteria Tsai, Yi-Chin Candace; Lapina, Maria Claribel; Bhushan, Shashi Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9883	journal	November 2015
CXCR4 signaling directs Igk recombination and the molecular mechanisms of late B lymphopoiesis Mandal, Malay; Okoreeh, Michael K.; Kennedy, Domenick E. Nature Immunology, Vol. 20, Issue 10 https://doi.org/10.1038/s41590-019-0468-0	journal	September 2019
The quest for atmospheric methane oxidizers in forest soils: Atmospheric methane-oxidizing methanotrophs in forest soils Kolb, Steffen Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00047.x	journal	July 2009
Expanding the Verrucomicrobial Methanotrophic World: Description of Three Novel Species of Methylacidimicrobium gen. nov. van Teeseling, Muriel C. F.; Pol, Arjan; Harhangi, Harry R. Applied and Environmental Microbiology, Vol. 80, Issue 21 https://doi.org/10.1128/AEM.01838-14	journal	August 2014
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts611	journal	October 2012
Rhizosphere bacteriome structure and functions Ling, Ning; Wang, Tingting; Kuzyakov, Yakov Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28448-9	journal	February 2022
Rhodomicrobium udaipurense sp. nov., a psychrotolerant, phototrophic alphaproteobacterium isolated from a freshwater stream Ramana, V. V.; Raj, P. S.; Tushar, L. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 7 https://doi.org/10.1099/ijs.0.046409-0	journal	January 2013
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
Characterization of Methanotrophic Bacterial Populations in Soils Showing Atmospheric Methane Uptake Holmes, Andrew J.; Roslev, Peter; McDonald, Ian R. Applied and Environmental Microbiology, Vol. 65, Issue 8 https://doi.org/10.1128/AEM.65.8.3312-3318.1999	journal	August 1999
Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1420797112	journal	April 2015
Model of the molecular basis for hydroxylamine oxidation and nitrous oxide production in methanotrophic bacteria: N-metabolism gene inventory in methanotrophic bacteria Campbell, Mark A.; Nyerges, Györgyi; Kozlowski, Jessica A. FEMS Microbiology Letters, Vol. 322, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02340.x	journal	July 2011
Ancient Permafrost and a Future, Warmer Arctic Froese, D. G.; Westgate, J. A.; Reyes, A. V. Science, Vol. 321, Issue 5896 https://doi.org/10.1126/science.1157525	journal	September 2008
Methane dynamics regulated by microbial community response to permafrost thaw McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B. Nature, Vol. 514, Issue 7523 https://doi.org/10.1038/nature13798	journal	October 2014
Revisiting life strategy concepts in environmental microbial ecology Ho, Adrian; Lonardo, D. Paolo Di; Bodelier, Paul L. E. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fix006	journal	January 2017
Acetate utilization as a survival strategy of peat-inhabiting Methylocystis spp.: Acetate utilization by Methylocystis spp. Belova, Svetlana E.; Baani, Mohamed; Suzina, Natalia E. Environmental Microbiology Reports, Vol. 3, Issue 1 https://doi.org/10.1111/j.1758-2229.2010.00180.x	journal	February 2011
Analysis of Permafrost Thermal Dynamics and Response to Climate Change in the CMIP5 Earth System Models Koven, Charles D.; Riley, William J.; Stern, Alex Journal of Climate, Vol. 26, Issue 6 https://doi.org/10.1175/JCLI-D-12-00228.1	journal	March 2013
Soil geochemistry confines microbial abundances across an arctic landscape; implications for net carbon exchange with the atmosphere Gray, N. D.; McCann, C. M.; Christgen, B. Biogeochemistry, Vol. 120, Issue 1-3 https://doi.org/10.1007/s10533-014-9997-7	journal	May 2014
Methanotrophy below pH 1 by a new Verrucomicrobia species Pol, Arjan; Heijmans, Klaas; Harhangi, Harry R. Nature, Vol. 450, Issue 7171 https://doi.org/10.1038/nature06222	journal	November 2007
Environmental Transcription of mmoX by Methane-Oxidizing Proteobacteria in a Subarctic Palsa Peatland Liebner, Susanne; Svenning, Mette M. Applied and Environmental Microbiology, Vol. 79, Issue 2 https://doi.org/10.1128/AEM.02292-12	journal	October 2012
Methane-cycling communities in a permafrost-affected soil on Herschel Island, Western Canadian Arctic: active layer profiling of mcrA and pmoA genes Barbier, Béatrice A.; Dziduch, Isabel; Liebner, Susanne FEMS Microbiology Ecology, Vol. 82, Issue 2 https://doi.org/10.1111/j.1574-6941.2012.01332.x	journal	March 2012
Heterologous expression of heterotrophic nitrification genes Crossman, L. C.; Moir, J. W. B.; Enticknap, J. J. Microbiology, Vol. 143, Issue 12 https://doi.org/10.1099/00221287-143-12-3775	journal	December 1997
Methylohalobius crimeensis gen. nov., sp. nov., a moderately halophilic, methanotrophic bacterium isolated from hypersaline lakes of Crimea Heyer, J. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 5 https://doi.org/10.1099/ijs.0.63213-0	journal	September 2005
Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea Ghosh, Wriddhiman; Dam, Bomba FEMS Microbiology Reviews, Vol. 33, Issue 6 https://doi.org/10.1111/j.1574-6976.2009.00187.x	journal	November 2009
Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2 Baani, M.; Liesack, W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 29 https://doi.org/10.1073/pnas.0702643105	journal	July 2008
Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes Vangelisti, Alberto; Guidi, Lucia; Cavallini, Andrea Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58878-8	journal	February 2020
Diversity of Aerobic Methanotrophic Bacteria in a Permafrost Active Layer Soil of the Lena Delta, Siberia Liebner, Susanne; Rublack, Katja; Stuehrmann, Torben Microbial Ecology, Vol. 57, Issue 1 https://doi.org/10.1007/s00248-008-9411-x	journal	July 2008
Biogeochemistry of Methane Exchange between Natural Wetlands and the Atmosphere Whalen, S. C. Environmental Engineering Science, Vol. 22, Issue 1 https://doi.org/10.1089/ees.2005.22.73	journal	January 2005
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
Metagenomic resolution of microbial functions in deep-sea hydrothermal plumes across the Eastern Lau Spreading Center Anantharaman, Karthik; Breier, John A.; Dick, Gregory J. The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.81	journal	June 2015
Effects of simulated spring thaw of permafrost from mineral cryosol on CO ₂ emissions and atmospheric CH ₄ uptake Stackhouse, Brandon T.; Vishnivetskaya, Tatiana A.; Layton, Alice Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 9 https://doi.org/10.1002/2015JG003004	journal	September 2015
Molecular Analyses of Novel Methanotrophic Communities in Forest Soil That Oxidize Atmospheric Methane Henckel, T.; Jackel, U.; Schnell, S. Applied and Environmental Microbiology, Vol. 66, Issue 5 https://doi.org/10.1128/aem.66.5.1801-1808.2000	journal	May 2000
Sulfate-reducing microorganisms in wetlands – fameless actors in carbon cycling and climate change Pester, Michael Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00072	journal	January 2012

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