Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils

Narrowe, Adrienne B.; Borton, Mikayla A.; Hoyt, David W.; Smith, Garrett J.; Daly, Rebecca A.; Angle, Jordan C.; Eder, Elizabeth K.; Wong, Allison R.; Wolfe, Richard A.; Pappas, Alexandra; Bohrer, Gil; Miller, Christopher S.; Wrighton, Kelly C.; Orsi, William

doi:10.1128/msystems.00320-19

Title: Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils

Journal Article · 03 December 2019 · mSystems

DOI: https://doi.org/10.1128/msystems.00320-19 · OSTI ID:1626180

^[1]; Borton, Mikayla A. ^[2]; Hoyt, David W. ^[3];

^[4]; Daly, Rebecca A. ^[2]; Angle, Jordan C. ^[4]; Eder, Elizabeth K. ^[3]; Wong, Allison R. ^[3]; Wolfe, Richard A. ^[4]; Pappas, Alexandra ^[4]; Bohrer, Gil ^[5];

^[6]; Wrighton, Kelly C. ^[7]; Orsi, William ^[8]

Colorado State Univ., Fort Collins, CO (United States). Dept. of Soil and Crop Sciences; DOE/OSTI
Colorado State Univ., Fort Collins, CO (United States). Dept. of Soil and Crop Sciences
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
The Ohio State Univ., Columbus, OH (United States), Dept. of Microbiology
The Ohio State Univ., Columbus, OH (United States), Dept. of Civil, Environmental & Geodetic Engineering
Univ. of Colorado Denver, Colorado (United States), Dept. of Integrative Biology
Colorado State Univ., Fort Collins, CO (United States), Dept. of Soil and Crop Sciences
Woods Hole Oceanographic Institution

Wetland soils are one of the largest natural contributors to the emission of methane, a potent greenhouse gas. Currently, microbial contributions to methane emissions from these systems emphasize the roles of acetoclastic and hydrogenotrophic methanogens, while less frequently considering methyl-group substrates (e.g., methanol and methylamines). Here, we integrated laboratory and field experiments to explore the potential for methylotrophic methanogenesis in Old Woman Creek (OWC), a temperate freshwater wetland located in Ohio, USA. We first demonstrated the capacity for methylotrophic methanogenesis in these soils using laboratory soil microcosms amended with trimethylamine. However, subsequent field porewater nuclear magnetic resonance (NMR) analyses to identify methanogenic substrates failed to detect evidence for methylamine compounds in soil porewaters, instead noting the presence of the methylotrophic substrate methanol. Accordingly, our wetland soil-derived metatranscriptomic data indicated that methanol utilization by theMethanomassiliicoccaceaewas the likely source of methylotrophic methanogenesis.Methanomassiliicoccaceaerelative contributions tomcrAtranscripts nearly doubled with depth, accounting for up to 8% of themcrAtranscripts in 25-cm-deep soils. Longitudinal 16S rRNA amplicon andmcrAgene surveys demonstrated thatMethanomassiliicoccaceaewere stably present over 2 years across lateral and depth gradients in this wetland. Meta-analysis of 16S rRNA sequences similar (>99%) to OWCMethanomassiliicoccaceaein public databases revealed a global distribution, with a high representation in terrestrial soils and sediments. Together, our results demonstrate that methylotrophic methanogenesis likely contributes to methane flux from climatically relevant wetland soils. IMPORTANCEUnderstanding the sources and controls on microbial methane production from wetland soils is critical to global methane emission predictions, particularly in light of changing climatic conditions. Current biogeochemical models of methanogenesis consider only acetoclastic and hydrogenotrophic sources and exclude methylotrophic methanogenesis, potentially underestimating microbial contributions to methane flux. Our multi-omic results demonstrated that methylotrophic methanogens of the familyMethanomassiliicoccaceaewere present and active in a freshwater wetland, with metatranscripts indicating that methanol, not methylamines, was the likely substrate under the conditions measured here. However, laboratory experiments indicated the potential for other methanogens to become enriched in response to trimethylamine, revealing the reservoir of methylotrophic methanogenesis potential residing in these soils. Collectively, our approach used coupled field and laboratory investigations to illuminate metabolisms influencing the terrestrial microbial methane cycle, thereby offering direction for increased realism in predictive process-oriented models of methane flux in wetland soils.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Battelle Memorial Institute, Columbus, OH (United States); Colorado State Univ., Fort Collins, CO (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); The Ohio State Univ., Columbus, OH (United States)

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

Contributing Organization:: EMSL, JGI

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0018022; SC0019746

OSTI ID:: 1626180

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 6 Vol. 4; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (137)

Sporomusa, a new genus of gram-negative anaerobic bacteria including Sporomusa sphaeroides spec. nov. and Sporomusa ovata spec. nov. M�ller, Bernhard; O�mer, Rolf; Howard, Bernard H. Archives of Microbiology, Vol. 139, Issue 4 https://doi.org/10.1007/bf00408385	journal	November 1984
Microbial methanol formation: A major end product of pectin metabolism Schink, Bernhard; Zeikus, J. G. Current Microbiology, Vol. 4, Issue 6 https://doi.org/10.1007/bf02605383	journal	November 1980
Methanol as the Primary Methanogenic and Acetogenic Precursor in the Cold Zoige Wetland at Tibetan Plateau Jiang, Na; Wang, Yanfen; Dong, Xiuzhu Microbial Ecology, Vol. 60, Issue 1 https://doi.org/10.1007/s00248-009-9602-0	journal	October 2009
Complete genome analysis of a novel iflavirus from a leaf beetle, Aulacophora lewisii Ye, Zhuang-Xin; Li, Yue-Hong; Chen, Jian-Ping Archives of Virology, Vol. 166, Issue 1 https://doi.org/10.1007/s00705-020-04859-1	journal	October 2020
Methane Emissions From Created Riverine Wetlands Nahlik, Amanda M.; Mitsch, William J. Wetlands, Vol. 30, Issue 4 https://doi.org/10.1007/s13157-010-0038-6	journal	April 2010
Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases Krzycki, Joseph A. Current Opinion in Chemical Biology, Vol. 8, Issue 5 https://doi.org/10.1016/j.cbpa.2004.08.012	journal	October 2004
Methylotrophic methanogenesis in Sphagnum-dominated peatland soils Zalman, C. A.; Meade, N.; Chanton, J. Soil Biology and Biochemistry, Vol. 118 https://doi.org/10.1016/j.soilbio.2017.11.025	journal	March 2018
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Bacterial metabolism of methylated amines and identification of novel methylotrophs in Movile Cave Wischer, Daniela; Kumaresan, Deepak; Johnston, Antonia The ISME Journal, Vol. 9, Issue 1 https://doi.org/10.1038/ismej.2014.102	journal	July 2014
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
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
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
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
High proportions of bacteria and archaea across most biomes remain uncultured Steen, Andrew D.; Crits-Christoph, Alexander; Carini, Paul The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0484-y	journal	August 2019
Microdiversity ensures the maintenance of functional microbial communities under changing environmental conditions García-García, Natalia; Tamames, Javier; Linz, Alexandra M. The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0487-8	journal	August 2019
Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions Angle, Jordan C.; Morin, Timothy H.; Solden, Lindsey M. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01753-4	journal	November 2017
The deep-subsurface sulfate reducer Desulfotomaculum kuznetsovii employs two methanol-degrading pathways Sousa, Diana Z.; Visser, Michael; van Gelder, Antonie H. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02518-9	journal	January 2018
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
New insights into the relationship between taste perception and oral microbiota composition Cattaneo, Camilla; Gargari, Giorgio; Koirala, Ranjan Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-40374-3	journal	March 2019
The complete chloroplast genome of Gleditsia sinensis and Gleditsia japonica: genome organization, comparative analysis, and development of taxon specific DNA mini-barcodes Tan, Wei; Gao, Han; Jiang, Weiling Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-73392-7	journal	October 2020
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha Ruan, Xiaoxian; Wang, Zhen; Su, Yingjuan Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-07198-0	journal	February 2022
Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales Borton, Mikayla A.; Hoyt, David W.; Roux, Simon Proceedings of the National Academy of Sciences, Vol. 115, Issue 28 https://doi.org/10.1073/pnas.1800155115	journal	June 2018
Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri. Hippe, H.; Caspari, D.; Fiebig, K. Proceedings of the National Academy of Sciences, Vol. 76, Issue 1 https://doi.org/10.1073/pnas.76.1.494	journal	January 1979
The growing role of methane in anthropogenic climate change Saunois, M.; Jackson, R. B.; Bousquet, P. Environmental Research Letters, Vol. 11, Issue 12 https://doi.org/10.1088/1748-9326/11/12/120207	journal	December 2016
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Letunic, I.; Bork, P. Bioinformatics, Vol. 23, Issue 1 https://doi.org/10.1093/bioinformatics/btl529	journal	October 2006
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences Söllinger, Andrea; Schwab, Clarissa; Weinmaier, Thomas FEMS Microbiology Ecology, Vol. 92, Issue 1 https://doi.org/10.1093/femsec/fiv149	journal	November 2015
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Unravelling the one-carbon metabolism of the acetogen S poromusa strain An4 by genome and proteome analysis: Unravelling one-carbon metabolism in Sporomusa An4 Visser, Michael; Pieterse, Mervin M.; Pinkse, Martijn W. H. Environmental Microbiology, Vol. 18, Issue 9 https://doi.org/10.1111/1462-2920.12973	journal	August 2015
High-resolution sequencing reveals unexplored archaeal diversity in freshwater wetland soils: Freshwater wetland archaeal diversity Narrowe, Adrienne B.; Angle, Jordan C.; Daly, Rebecca A. Environmental Microbiology, Vol. 19, Issue 6 https://doi.org/10.1111/1462-2920.13703	journal	March 2017
Methanol metabolism in the acetogenic bacterium Acetobacterium woodii Kremp, Florian; Poehlein, Anja; Daniel, Rolf Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14356	journal	October 2018
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales Bridgham, Scott D.; Cadillo-Quiroz, Hinsby; Keller, Jason K. Global Change Biology, Vol. 19, Issue 5 https://doi.org/10.1111/gcb.12131	journal	February 2013
Methanogen community in Zoige wetland of Tibetan plateau and phenotypic characterization of a dominant uncultured methanogen cluster ZC-I Zhang, Guishan; Tian, Jianqing; Jiang, Na Environmental Microbiology, Vol. 10, Issue 7 https://doi.org/10.1111/j.1462-2920.2008.01606.x	journal	July 2008
Acetate threshold values and acetate activating enzymes in methanogenic bacteria Jetten, Mike S. M.; Stams, Alfons J. M.; Zehnder, Alexander J. B. FEMS Microbiology Letters, Vol. 73, Issue 4 https://doi.org/10.1111/j.1574-6968.1990.tb03958.x	journal	June 1990
Extremely halophilic, methylotrophic, anaerobic bacteria Zhilina, Tatyana N.; Zavarzin, George A. FEMS Microbiology Letters, Vol. 87, Issue 3-4 https://doi.org/10.1111/j.1574-6968.1990.tb04930.x	journal	December 1990
Aerobic methanol-oxidizing Bacteria â€ƒin soil Kolb, Steffen FEMS Microbiology Letters, Vol. 300, Issue 1 https://doi.org/10.1111/j.1574-6968.2009.01681.x	journal	November 2009
Freshwater Methane Emissions Offset the Continental Carbon Sink Bastviken, D.; Tranvik, L. J.; Downing, J. A. Science, Vol. 331, Issue 6013 https://doi.org/10.1126/science.1196808	journal	January 2011
A global atlas of the dominant bacteria found in soil Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E. Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aap9516	journal	January 2018
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
Stable Carbon Isotope Fractionation by Methylotrophic Methanogenic Archaea Penger, Jörn; Conrad, Ralf; Blaser, Martin Applied and Environmental Microbiology, Vol. 78, Issue 21 https://doi.org/10.1128/aem.01773-12	journal	August 2012
“Methanoplasmatales,” Thermoplasmatales-Related Archaea in Termite Guts and Other Environments, Are the Seventh Order of Methanogens Paul, Kristina; Nonoh, James O.; Mikulski, Lena Applied and Environmental Microbiology, Vol. 78, Issue 23 https://doi.org/10.1128/aem.02193-12	journal	September 2012
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
Methanogenesis from Methanol and Methylamines and Acetogenesis from Hydrogen and Carbon Dioxide in the Sediments of a Eutrophic Lake † Lovley, Derek R.; Klug, Michael J. Applied and Environmental Microbiology, Vol. 45, Issue 4 https://doi.org/10.1128/aem.45.4.1310-1315.1983	journal	January 1983
Methane Metabolism in a Temperate Swamp Amaral, J. A.; Knowles, R. Applied and Environmental Microbiology, Vol. 60, Issue 11 https://doi.org/10.1128/aem.60.11.3945-3951.1994	journal	January 1994
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
Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity Shade, A.; Jones, S. E.; Caporaso, J. G. mBio, Vol. 5, Issue 4 https://doi.org/10.1128/mbio.01371-14	journal	July 2014
A “Cultural” Renaissance: Genomics Breathes New Life into an Old Craft Carini, Paul mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/msystems.00092-19	journal	May 2019
Growth Characteristics of Methanomassiliicoccus luminyensis and Expression of Methyltransferase Encoding Genes Kröninger, Lena; Gottschling, Jacqueline; Deppenmeier, Uwe Archaea, Vol. 2017 https://doi.org/10.1155/2017/2756573	journal	January 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine Borrel, Guillaume; Parisot, Nicolas; Harris, Hugh MB BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-679	journal	January 2014
The complete genome sequence of the methanogenic archaeon ISO4-H5 provides insights into the methylotrophic lifestyle of a ruminal representative of the Methanomassiliicoccales Li, Yang; Leahy, Sinead C.; Jeyanathan, Jeyamalar Standards in Genomic Sciences, Vol. 11, Issue 1 https://doi.org/10.1186/s40793-016-0183-5	journal	September 2016
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM Riley, W. J.; Subin, Z. M.; Lawrence, D. M. Biogeosciences, Vol. 8, Issue 7 https://doi.org/10.5194/bg-8-1925-2011	journal	January 2011
Methane Feedbacks to the Global Climate System in a Warmer World Dean, Joshua F.; Middelburg, Jack J.; Röckmann, Thomas Reviews of Geophysics, Vol. 56, Issue 1 https://doi.org/10.1002/2017RG000559	journal	March 2018
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Data Analysis Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4_9	book	June 2016
Sporomusa, a new genus of gram-negative anaerobic bacteria including Sporomusa sphaeroides spec. nov. and Sporomusa ovata spec. nov. M�ller, Bernhard; O�mer, Rolf; Howard, Bernard H. Archives of Microbiology, Vol. 139, Issue 4 https://doi.org/10.1007/BF00408385	journal	November 1984
Microbial methanol formation: A major end product of pectin metabolism Schink, Bernhard; Zeikus, J. G. Current Microbiology, Vol. 4, Issue 6 https://doi.org/10.1007/BF02605383	journal	November 1980
Methanol as the Primary Methanogenic and Acetogenic Precursor in the Cold Zoige Wetland at Tibetan Plateau Jiang, Na; Wang, Yanfen; Dong, Xiuzhu Microbial Ecology, Vol. 60, Issue 1 https://doi.org/10.1007/s00248-009-9602-0	journal	October 2009
Methane Emissions From Created Riverine Wetlands Nahlik, Amanda M.; Mitsch, William J. Wetlands, Vol. 30, Issue 4 https://doi.org/10.1007/s13157-010-0038-6	journal	April 2010
Acetate threshold values and acetate activating enzymes in methanogenic bacteria Jetten, M. FEMS Microbiology Letters, Vol. 73, Issue 4 https://doi.org/10.1016/0378-1097(90)90768-L	journal	June 1990
Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. Jetten, M. FEMS Microbiology Letters, Vol. 88, Issue 3-4 https://doi.org/10.1016/0378-1097(92)90802-U	journal	June 1992
Simulation of methanogenesis in the mathematical model ecosys Grant, R. F. Soil Biology and Biochemistry, Vol. 30, Issue 7 https://doi.org/10.1016/S0038-0717(97)00218-6	journal	July 1998
Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases Krzycki, Joseph A. Current Opinion in Chemical Biology, Vol. 8, Issue 5 https://doi.org/10.1016/j.cbpa.2004.08.012	journal	October 2004
Production and consumption of methane in freshwater lake ecosystems Borrel, Guillaume; Jézéquel, Didier; Biderre-Petit, Corinne Research in Microbiology, Vol. 162, Issue 9 https://doi.org/10.1016/j.resmic.2011.06.004	journal	November 2011
In-depth analysis of core methanogenic communities from high elevation permafrost-affected wetlands Yang, Sizhong; Liebner, Susanne; Winkel, Matthias Soil Biology and Biochemistry, Vol. 111 https://doi.org/10.1016/j.soilbio.2017.03.007	journal	August 2017
Methylotrophic methanogenesis in Sphagnum-dominated peatland soils Zalman, C. A.; Meade, N.; Chanton, J. Soil Biology and Biochemistry, Vol. 118 https://doi.org/10.1016/j.soilbio.2017.11.025	journal	March 2018
Data Analysis Cayrel, R. Symposium - International Astronomical Union, Vol. 132 https://doi.org/10.1017/s0074180900035269	journal	January 1988
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Bacterial metabolism of methylated amines and identification of novel methylotrophs in Movile Cave Wischer, Daniela; Kumaresan, Deepak; Johnston, Antonia The ISME Journal, Vol. 9, Issue 1 https://doi.org/10.1038/ismej.2014.102	journal	July 2014
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
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
ModelFinder: fast model selection for accurate phylogenetic estimates Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F. Nature Methods, Vol. 14, Issue 6 https://doi.org/10.1038/nmeth.4285	journal	May 2017
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
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
High proportions of bacteria and archaea across most biomes remain uncultured Steen, Andrew D.; Crits-Christoph, Alexander; Carini, Paul The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0484-y	journal	August 2019
Microdiversity ensures the maintenance of functional microbial communities under changing environmental conditions García-García, Natalia; Tamames, Javier; Linz, Alexandra M. The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0487-8	journal	August 2019
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E. The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00921-1	journal	March 2021
Methanogenesis in oxygenated soils is a substantial fraction of wetland methane emissions Angle, Jordan C.; Morin, Timothy H.; Solden, Lindsey M. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01753-4	journal	November 2017
The deep-subsurface sulfate reducer Desulfotomaculum kuznetsovii employs two methanol-degrading pathways Sousa, Diana Z.; Visser, Michael; van Gelder, Antonie H. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02518-9	journal	January 2018
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao Nature Microbiology, Vol. 3, Issue 4 https://doi.org/10.1038/s41564-018-0129-3	journal	March 2018
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R. Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0209-9	journal	July 2019
Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales Borton, Mikayla A.; Hoyt, David W.; Roux, Simon Proceedings of the National Academy of Sciences, Vol. 115, Issue 28 https://doi.org/10.1073/pnas.1800155115	journal	June 2018
Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri. Hippe, H.; Caspari, D.; Fiebig, K. Proceedings of the National Academy of Sciences, Vol. 76, Issue 1 https://doi.org/10.1073/pnas.76.1.494	journal	January 1979
The growing role of methane in anthropogenic climate change Saunois, M.; Jackson, R. B.; Bousquet, P. Environmental Research Letters, Vol. 11, Issue 12 https://doi.org/10.1088/1748-9326/11/12/120207	journal	December 2016
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation Letunic, I.; Bork, P. Bioinformatics, Vol. 23, Issue 1 https://doi.org/10.1093/bioinformatics/btl529	journal	October 2006
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth Peng, Y.; Leung, H. C. M.; Yiu, S. M. Bioinformatics, Vol. 28, Issue 11 https://doi.org/10.1093/bioinformatics/bts174	journal	April 2012
Phylogenetic and genomic analysis of Methanomassiliicoccales in wetlands and animal intestinal tracts reveals clade-specific habitat preferences Söllinger, Andrea; Schwab, Clarissa; Weinmaier, Thomas FEMS Microbiology Ecology, Vol. 92, Issue 1 https://doi.org/10.1093/femsec/fiv149	journal	November 2015
Complex Evolutionary History of Translation Elongation Factor 2 and Diphthamide Biosynthesis in Archaea and Parabasalids Narrowe, Adrienne B.; Spang, Anja; Stairs, Courtney W. Genome Biology and Evolution, Vol. 10, Issue 9 https://doi.org/10.1093/gbe/evy154	journal	August 2018
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
UFBoot2: Improving the Ultrafast Bootstrap Approximation Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 35, Issue 2 https://doi.org/10.1093/molbev/msx281	journal	October 2017
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Systematic Biology, Vol. 59, Issue 3 https://doi.org/10.1093/sysbio/syq010	journal	March 2010
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
Unravelling the one-carbon metabolism of the acetogen S poromusa strain An4 by genome and proteome analysis: Unravelling one-carbon metabolism in Sporomusa An4 Visser, Michael; Pieterse, Mervin M.; Pinkse, Martijn W. H. Environmental Microbiology, Vol. 18, Issue 9 https://doi.org/10.1111/1462-2920.12973	journal	August 2015
High-resolution sequencing reveals unexplored archaeal diversity in freshwater wetland soils: Freshwater wetland archaeal diversity Narrowe, Adrienne B.; Angle, Jordan C.; Daly, Rebecca A. Environmental Microbiology, Vol. 19, Issue 6 https://doi.org/10.1111/1462-2920.13703	journal	March 2017
Thermodynamically diverse syntrophic aromatic compound catabolism: Thermodynamically diverse syntrophic catabolism Nobu, Masaru Konishi; Narihiro, Takashi; Liu, Miaomiao Environmental Microbiology, Vol. 19, Issue 11 https://doi.org/10.1111/1462-2920.13922	journal	October 2017
Increases in temperature and nutrient availability positively affect methane‐cycling microorganisms in Arctic thermokarst lake sediments de Jong, Anniek E. E.; in ’t Zandt, Michiel H.; Meisel, Ove H. Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14345	journal	September 2018
Methanol metabolism in the acetogenic bacterium Acetobacterium woodii Kremp, Florian; Poehlein, Anja; Daniel, Rolf Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14356	journal	October 2018
Microbial trimethylamine metabolism in marine environments: Microbial TMA metabolism Sun, Jing; Mausz, Michaela A.; Chen, Yin Environmental Microbiology, Vol. 21, Issue 2 https://doi.org/10.1111/1462-2920.14461	journal	December 2018
Comparative genomics and physiology of the genus Methanohalophilus , a prevalent methanogen in hydraulically fractured shale Borton, Mikayla A.; Daly, Rebecca A.; O'Banion, Bridget Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14467	journal	December 2018
Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales Bridgham, Scott D.; Cadillo-Quiroz, Hinsby; Keller, Jason K. Global Change Biology, Vol. 19, Issue 5 https://doi.org/10.1111/gcb.12131	journal	February 2013
Methanogen community in Zoige wetland of Tibetan plateau and phenotypic characterization of a dominant uncultured methanogen cluster ZC-I Zhang, Guishan; Tian, Jianqing; Jiang, Na Environmental Microbiology, Vol. 10, Issue 7 https://doi.org/10.1111/j.1462-2920.2008.01606.x	journal	July 2008
Extremely halophilic, methylotrophic, anaerobic bacteria Zhilina, Tatyana N.; Zavarzin, George A. FEMS Microbiology Letters, Vol. 87, Issue 3-4 https://doi.org/10.1111/j.1574-6968.1990.tb04930.x	journal	December 1990
Aerobic methanol-oxidizing Bacteria â€ƒin soil Kolb, Steffen FEMS Microbiology Letters, Vol. 300, Issue 1 https://doi.org/10.1111/j.1574-6968.2009.01681.x	journal	November 2009
Freshwater Methane Emissions Offset the Continental Carbon Sink Bastviken, D.; Tranvik, L. J.; Downing, J. A. Science, Vol. 331, Issue 6013 https://doi.org/10.1126/science.1196808	journal	January 2011
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
A global atlas of the dominant bacteria found in soil Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E. Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aap9516	journal	January 2018
Wetland Sediments Host Diverse Microbial Taxa Capable of Cycling Alcohols Dalcin Martins, Paula; Frank, Jeroen; Mitchell, Hugh Applied and Environmental Microbiology, Vol. 85, Issue 12 https://doi.org/10.1128/AEM.00189-19	journal	April 2019
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
Methanogenesis from Methanol at Low Temperatures by a Novel Psychrophilic Methanogen, "Methanolobus psychrophilus" sp. nov., Prevalent in Zoige Wetland of the Tibetan Plateau Zhang, G.; Jiang, N.; Liu, X. Applied and Environmental Microbiology, Vol. 74, Issue 19 https://doi.org/10.1128/AEM.01146-08	journal	August 2008
Stable Carbon Isotope Fractionation by Methylotrophic Methanogenic Archaea Penger, Jörn; Conrad, Ralf; Blaser, Martin Applied and Environmental Microbiology, Vol. 78, Issue 21 https://doi.org/10.1128/AEM.01773-12	journal	August 2012
“Methanoplasmatales,” Thermoplasmatales-Related Archaea in Termite Guts and Other Environments, Are the Seventh Order of Methanogens Paul, Kristina; Nonoh, James O.; Mikulski, Lena Applied and Environmental Microbiology, Vol. 78, Issue 23 https://doi.org/10.1128/AEM.02193-12	journal	September 2012
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
Methanogenesis from Methanol and Methylamines and Acetogenesis from Hydrogen and Carbon Dioxide in the Sediments of a Eutrophic Lake † Lovley, Derek R.; Klug, Michael J. Applied and Environmental Microbiology, Vol. 45, Issue 4 https://doi.org/10.1128/aem.45.4.1310-1315.1983	journal	January 1983
Methane Metabolism in a Temperate Swamp Amaral, J. A.; Knowles, R. Applied and Environmental Microbiology, Vol. 60, Issue 11 https://doi.org/10.1128/aem.60.11.3945-3951.1994	journal	January 1994
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
Members of the Genus Methylobacter Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland Smith, Garrett J.; Angle, Jordan C.; Solden, Lindsey M. mBio, Vol. 9, Issue 6 https://doi.org/10.1128/mBio.00815-18	journal	November 2018
Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity Shade, A.; Jones, S. E.; Caporaso, J. G. mBio, Vol. 5, Issue 4 https://doi.org/10.1128/mBio.01371-14	journal	July 2014
A “Cultural” Renaissance: Genomics Breathes New Life into an Old Craft Carini, Paul mSystems, Vol. 4, Issue 3 https://doi.org/10.1128/mSystems.00092-19	journal	May 2019
Growth Characteristics of Methanomassiliicoccus luminyensis and Expression of Methyltransferase Encoding Genes Kröninger, Lena; Gottschling, Jacqueline; Deppenmeier, Uwe Archaea, Vol. 2017 https://doi.org/10.1155/2017/2756573	journal	January 2017
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine Borrel, Guillaume; Parisot, Nicolas; Harris, Hugh MB BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-679	journal	January 2014
Metagenomic biomarker discovery and explanation Segata, Nicola; Izard, Jacques; Waldron, Levi Genome Biology, Vol. 12, Issue 6 https://doi.org/10.1186/gb-2011-12-6-r60	journal	January 2011
The complete genome sequence of the methanogenic archaeon ISO4-H5 provides insights into the methylotrophic lifestyle of a ruminal representative of the Methanomassiliicoccales Li, Yang; Leahy, Sinead C.; Jeyanathan, Jeyamalar Standards in Genomic Sciences, Vol. 11, Issue 1 https://doi.org/10.1186/s40793-016-0183-5	journal	September 2016
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent ETH Zurich https://doi.org/10.3929/ethz-b-000025281	text	January 2010
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0 Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent Oxford University Press https://doi.org/10.5167/uzh-155669	text	January 2010
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM Riley, W. J.; Subin, Z. M.; Lawrence, D. M. Biogeosciences, Vol. 8, Issue 7 https://doi.org/10.5194/bg-8-1925-2011	journal	January 2011
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM Riley, W. J.; Subin, Z. M.; Lawrence, D. M. Biogeosciences Discussions, Vol. 8, Issue 1 https://doi.org/10.5194/bgd-8-1733-2011	journal	January 2011
The complete genome sequence of the methanogenic archaeon ISO4-H5 provides insights into the methylotrophic lifestyle of a ruminal representative of the Methanomassiliicoccales Li, Yang; Leahy, Sinead; Jeyanathan, Jeyamalar figshare https://doi.org/10.6084/m9.figshare.c.3597134.v1	collection	January 2016
Metabolic marker gene mining provides insight in global mcrA diversity and, coupled with targeted genome reconstruction, sheds further light on metabolic potential of the Methanomassiliicoccales Speth, Daan R.; Orphan, Victoria J. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5614	journal	January 2018

Similar Records

Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils

Journal Article · 2019 · mSystems · OSTI ID:1770578

Narrowe, Adrienne B.; Borton, Mikayla; Hoyt, David W.; +10 more

Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost

Journal Article · 2023 · mSystems · OSTI ID:2377155

Ellenbogen, Jared B.; Borton, Mikayla A.; McGivern, Bridget B.; +13 more

Members of the Genus Methylobacter Are Inferred To Account for the Majority of Aerobic Methane Oxidation in Oxic Soils from a Freshwater Wetland

Journal Article · 2018 · mBio (Online) · OSTI ID:1481031

Smith, Garrett J.; Angle, Jordan C.; Solden, Lindsey M.; +10 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
Microbiology

Title: Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils

Citation Formats

References (137)

Similar Records

Related Subjects