Diverse and unconventional methanogens, methanotrophs, and methylotrophs in metagenome-assembled genomes from subsurface sediments of the Slate River floodplain, Crested Butte, CO, USA

Rasmussen, Anna N.; Tolar, Bradley B.; Bargar, John R.; Boye, Kristin; Francis, Christopher A.

doi:10.1128/msystems.00314-24

Diverse and unconventional methanogens, methanotrophs, and methylotrophs in metagenome-assembled genomes from subsurface sediments of the Slate River floodplain, Crested Butte, CO, USA

Journal Article · Fri Jun 28 00:00:00 EDT 2024 · mSystems

DOI:https://doi.org/10.1128/msystems.00314-24· OSTI ID:2376901

^[1]; ^[2]; Bargar, John R. ^[3]; Boye, Kristin ^[4]; ^[5]

Department of Earth System Science, Stanford University, Stanford, California, USA; SLAC National Accelerator Laboratory, Menlo Park, California, USA; Stanford University
Department of Earth System Science, Stanford University, Stanford, California, USA
Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA
SLAC National Accelerator Laboratory, Menlo Park, California, USA
Department of Earth System Science, Stanford University, Stanford, California, USA; Oceans Department, Stanford University, Stanford, California, USA

We use metagenome-assembled genomes (MAGs) to understand single-carbon (C1) compound-cycling—particularly methane-cycling—microorganisms in montane riparian floodplain sediments. We generated 1,233 MAGs (>50% completeness and <10% contamination) from 50- to 150-cm depth below the sediment surface capturing the transition between oxic, unsaturated sediments and anoxic, saturated sediments in the Slate River (SR) floodplain (Crested Butte, CO, USA). We recovered genomes of putative methanogens, methanotrophs, and methylotrophs (n = 57). Methanogens, found only in deep, anoxic depths at SR, originate from three different clades (Methanoregulaceae, Methanotrichaceae, and Methanomassiliicoccales), each with a different methanogenesis pathway; putative methanotrophic MAGs originate from within the Archaea (Candidatus Methanoperedens) in anoxic depths and uncultured bacteria (Ca. Binatia) in oxic depths. Genomes for canonical aerobic methanotrophs were not recovered. Ca. Methanoperedens were exceptionally abundant (~1,400× coverage, >50% abundance in the MAG library) in one sample that also contained aceticlastic methanogens, indicating a potential C1/methane-cycling hotspot. Ca. Methylomirabilis MAGs from SR encode pathways for methylotrophy but do not harbor methane monooxygenase or nitrogen reduction genes. Comparative genomic analysis supports that one clade within the Ca. Methylomirabilis genus is not methanotrophic. The genetic potential for methylotrophy was widespread, with over 10% and 19% of SR MAGs encoding a methanol dehydrogenase or substrate-specific methyltransferase, respectively. MAGs from uncultured Thermoplasmata archaea in the Ca. Gimiplasmatales (UBA10834) contain pathways that may allow for anaerobic methylotrophic acetogenesis. Overall, MAGs from SR floodplain sediments reveal a potential for methane production and consumption in the system and a robust potential for methylotrophy.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth & Environmental Systems Science (EESS); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 2376901

Alternate ID(s):: OSTI ID: 2440048

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 7 Vol. 9; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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