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

Ellenbogen, Jared B.; Borton, Mikayla A.; McGivern, Bridget B.; Cronin, Dylan R.; Hoyt, David W.; Freire-Zapata, Viviana; McCalley, Carmody K.; Varner, Ruth K.; Crill, Patrick M.; Wehr, Richard A.; Chanton, Jeffrey P.; Woodcroft, Ben J.; Tfaily, Malak M.; Tyson, Gene W.; Rich, Virginia I.; Wrighton, Kelly C.

doi:10.1128/msystems.00698-23

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

Journal Article · Thu Dec 07 23:00:00 EST 2023 · mSystems

DOI: https://doi.org/10.1128/msystems.00698-23 · OSTI ID:2377155

^[1]; Borton, Mikayla A. ^[1]; McGivern, Bridget B. ^[1]; Cronin, Dylan R. ^[2];

^[3]; Freire-Zapata, Viviana ^[4]; McCalley, Carmody K. ^[5];

^[6]; Crill, Patrick M. ^[7]; Wehr, Richard A. ^[4];

^[8];

^[9];

^[4]; Tyson, Gene W. ^[9]; Rich, Virginia I. ^[2];

^[1]

Colorado State Univ., Fort Collins, CO (United States)
The Ohio State Univ., Columbus, OH (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Univ. of Arizona, Tucson, AZ (United States)
Rochester Inst. of Technology, Rochester, NY (United States)
Univ. of New Hampshire, Durham, NH (United States)
Stockholm Univ. (Sweden)
Florida State Univ., Tallahassee, FL (United States)
Queensland University of Technology (QUT), Woolloongabba, QLD (Australia)

While wetlands are major sources of biogenic methane (CH₄), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH₄ emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methanogenesis in the thawing permafrost peatland of Stordalen Mire in Arctic Sweden. In quadrupling the genomic representation of the site’s methanogens and examining their encoded metabolism, we revealed that nearly 20% of the metagenome-assembled genomes (MAGs) encoded the potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; for Methanosarcinales and Methanobacteriales MAGs, these data indicated the use of methylated oxygen compounds (e.g., methanol), while for Methanomassiliicoccales, they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1,700 bacterial MAGs across 19 phyla encoded anaerobic methylotrophic potential, with expression across 12 phyla. Metabolomic analyses revealed the presence of diverse methylated compounds in the Mire, including some known methylotrophic substrates. Active methylotrophy was observed across all stages of a permafrost thaw gradient in Stordalen, with the most frozen non-methanogenic palsa found to host bacterial methylotrophy and the partially thawed bog and fully thawed fen seen to house both methanogenic and bacterial methylotrophic activities. Methanogenesis across increasing permafrost thaw is thus revised from the sole dominance of hydrogenotrophic production and the appearance of acetoclastic at full thaw to consider the co-occurrence of methylotrophy throughout. Collectively, these findings indicate that methanogenic and bacterial methylotrophy may be an important and previously underappreciated component of carbon cycling and emissions in these rapidly changing wetland habitats.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

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

Grant/Contract Number:: AC05-76RL01830; AC02-05CH11231; SC0023084; SC0023456

OSTI ID:: 2377155

Report Number(s):: PNNL-SA--189609

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 1 Vol. 9; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Characterization of a Three-Component Vanillate O-Demethylase from Moorella thermoacetica Naidu, D.; Ragsdale, S. W. Journal of Bacteriology, Vol. 183, Issue 11 https://doi.org/10.1128/JB.183.11.3276-3281.2001	journal	June 2001
Utilization of Methanol plus Hydrogen by Methanosarcina barkeri for Methanogenesis and Growth Müller, Volker; Blaut, Michael; Gottschalk, Gerhard Applied and Environmental Microbiology, Vol. 52, Issue 2 https://doi.org/10.1128/aem.52.2.269-274.1986	journal	August 1986
Isolation and characterization of acetyl-coenzyme A synthetase from Methanothrix soehngenii. Jetten, M. S.; Stams, A. J.; Zehnder, A. J. Journal of Bacteriology, Vol. 171, Issue 10 https://doi.org/10.1128/jb.171.10.5430-5435.1989	journal	October 1989
Reconstitution of trimethylamine-dependent coenzyme M methylation with the trimethylamine corrinoid protein and the isozymes of methyltransferase II from Methanosarcina barkeri. Ferguson, D. J.; Krzycki, J. A. Journal of Bacteriology, Vol. 179, Issue 3 https://doi.org/10.1128/jb.179.3.846-852.1997	journal	February 1997
Patterns in Wetland Microbial Community Composition and Functional Gene Repertoire Associated with Methane Emissions He, Shaomei; Malfatti, Stephanie A.; McFarland, Jack W. mBio, Vol. 6, Issue 3 https://doi.org/10.1128/mBio.00066-15	journal	May 2015
Uncovering the Diversity and Activity of Methylotrophic Methanogens in Freshwater Wetland Soils Narrowe, Adrienne B.; Borton, Mikayla A.; Hoyt, David W. mSystems, Vol. 4, Issue 6 https://doi.org/10.1128/mSystems.00320-19	journal	December 2019
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
Gene length corrected trimmed mean of M-values (GeTMM) processing of RNA-seq data performs similarly in intersample analyses while improving intrasample comparisons Smid, Marcel; Coebergh van den Braak, Robert R. J.; van de Werken, Harmen J. G. BMC Bioinformatics, Vol. 19, Issue 1 https://doi.org/10.1186/s12859-018-2246-7	journal	June 2018
MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis Uritskiy, Gherman V.; DiRuggiero, Jocelyne; Taylor, James Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0541-1	journal	September 2018
A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments Jones, Helen J.; Kröber, Eileen; Stephenson, Jason Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0732-4	journal	August 2019
Genomic and transcriptomic insights into methanogenesis potential of novel methanogens from mangrove sediments Zhang, Cui-Jing; Pan, Jie; Liu, Yang Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00876-z	journal	June 2020
The standard operating procedure of the DOE-JGI Metagenome Annotation Pipeline (MAP v.4) Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos Standards in Genomic Sciences, Vol. 11, Issue 1 https://doi.org/10.1186/s40793-016-0138-x	journal	February 2016
Genomic Characterization of Methanomicrobiales Reveals Three Classes of Methanogens Anderson, Iain; Ulrich, Luke E.; Lupa, Boguslaw PLoS ONE, Vol. 4, Issue 6 https://doi.org/10.1371/journal.pone.0005797	journal	June 2009
Activation of Methanogenesis in Arid Biological Soil Crusts Despite the Presence of Oxygen Angel, Roey; Matthies, Diethart; Conrad, Ralf PLoS ONE, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pone.0020453	journal	May 2011
Examination of the Glycine Betaine-Dependent Methylotrophic Methanogenesis Pathway: Insights Into Anaerobic Quaternary Amine Methylotrophy Creighbaum, Adam J.; Ticak, Tomislav; Shinde, Shrameeta Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02572	journal	November 2019
Methanol in Plant Life Dorokhov, Yuri L.; Sheshukova, Ekaterina V.; Komarova, Tatiana V. Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01623	journal	November 2018
Wetland restoration and methanogenesis: the activity of microbial populations and competition for substrates at different temperatures Jerman, V.; Metje, M.; Mandić-Mulec, I. Biogeosciences, Vol. 6, Issue 6 https://doi.org/10.5194/bg-6-1127-2009	journal	January 2009
FLUXNET-CH₄: a global, multi-ecosystem dataset and analysis of methane seasonality from freshwater wetlands Delwiche, Kyle B.; Knox, Sara Helen; Malhotra, Avni Earth System Science Data, Vol. 13, Issue 7 https://doi.org/10.5194/essd-13-3607-2021	journal	January 2021
EMERGE 2016 Autochamber Sites NMR Hoyt, David; Daly, Rebecca; McGivern, Bridget Zenodo https://doi.org/10.5281/zenodo.7519683	dataset	January 2023
EMERGE 2016 Autochamber Sites LC-MS Freire Zapata, Viviana; McGivern, Bridget; Daly, Rebecca Zenodo https://doi.org/10.5281/zenodo.7519815	dataset	January 2023
Metagenome-Assembled Genome DRAM Annotations (EMERGE 97% dereplicated MAGs) McGivern, Bridget; Cronin, Dylan; Institute, NSF EMERGE Biology Integration Zenodo https://doi.org/10.5281/zenodo.7587534	dataset	January 2023
Stordalen Mire July 2016 Metatranscriptome Data from McGivern et al. McGivern, Bridget Zenodo https://doi.org/10.5281/zenodo.7591900	dataset	January 2023
Metagenome-assembled genomes (MAGs) from Stordalen Mire, Sweden Cronin, Dylan; Institute, NSF EMERGE Biology Integration Zenodo https://doi.org/10.5281/zenodo.7596016	dataset	January 2023
EMERGE Sample Metadata Sheet for Samples with Microbiomes Hodgkins, Suzanne; Wilson, Rachel; Chanton, Jeffrey Zenodo https://doi.org/10.5281/zenodo.7720573	dataset	January 2022
Newick Trees for EMERGE methanogen genome tree, and methylotrophic gene trees Jared B. Ellenbogen, Mikayla A. Borton Zenodo https://doi.org/10.5281/zenodo.7864933	dataset	January 2023
Autochamber CH4 Fluxes and δ13C Values at Stordalen Mire McCalley, Carmody K. Zenodo https://doi.org/10.5281/zenodo.7897922	dataset	January 2023
GroopM: an automated tool for the recovery of population genomes from related metagenomes Imelfort, Michael; Parks, Donovan; Woodcroft, Ben J. PeerJ, Vol. 2 https://doi.org/10.7717/peerj.603	journal	January 2014
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019

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