Targeted curation of the gut microbial gene content modulating human cardiovascular disease

Borton, Mikayla A.; Shaffer, Michael J.; Hoyt, David; Jiang, Ruisheng; Ellenbogen, Jared; Purvine, Samuel O.; Nicora, Carrie; Eder, Elizabeth K.; Wong, Allison R.; Smulian, A. George; Lipton, Mary; Krzycki, Joseph A.; Wrighton, Kelly

doi:10.1101/2022.06.20.496735

Cited by 4 publications

(2 citation statements)

References 77 publications

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“…For example, four functionally unique quaternary amine-dependent methyltransferases have been biochemically characterized and are shown to demethylate distinct substrates ( 30 , 33 , 35 , 38 ), but only one of these is present in the KEGG database ( 30 ). As a result, the accurate functional assignment of these genes often requires paired non-homology-based methods, including gene synteny ( 19 , 30 , 33 , 38 , 62 ), unique residues ( 54 , 62 ), and phylogeny ( 62 ) to confirm gene functional assignments.…”

Section: Discussionmentioning

confidence: 99%

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

Ellenbogen,

Borton,

McGivern

et al. 2024

mSystems

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While wetlands are major sources of biogenic methane (CH 4 ), our understanding of resident microbial metabolism is incomplete, which compromises the prediction of CH 4 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. IMPORTANCE Wetlands are the biggest natural source of atmospheric methane (CH 4 ) emissions, yet we have an incomplete understanding of the suite of microbial metabolism that results in CH 4 formation. Specifically, methanogenesis from methylated compounds is excluded from all ecosystem models used to predict wetland contributions to the global CH 4 budget. Though recent studies have shown methylotrophic methanogenesis to be active across wetlands, the broad climatic importance of the metabolism remains critically understudied. Further, some methylotrophic bacteria are known to produce methanogenic by-products like acetate, increasing the complexity of the microbial methylotrophic metabolic network. Prior studies of Stordalen Mire have suggested that methylotrophic methanogenesis is irrelevant in situ and have not emphasized the bacterial capacity for metabolism, both of which we countered in this study. The importance of our findings lies in the significant advancement toward unraveling the broader impact of methylotrophs in wetland methanogenesis and, consequently, their contribution to the terrestrial global carbon cycle.

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Section: Discussionmentioning

confidence: 99%

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

Ellenbogen,

Borton,

McGivern

et al. 2024

mSystems

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“…We also sequenced 9 samples from laboratory enrichments that are released in this study. Two of these enrichment samples were sequenced at The Ohio State University Genomic Shared Resource Facility with library preparation Nextera XT library system and sequencing done on HiSeq 2500 using methods described in more detail (11). An additional 7 laboratory enrichments were sequenced in 2018 from Genomics and Microarray Shared Resource at University of Colorado Denver Cancer Center, Denver, CO, USA.…”

Section: Methodsmentioning

confidence: 99%

Mapping the soil microbiome functions shaping wetland methane emissions

Oliverio,

Narrowe,

Villa

et al. 2024

Preprint

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Despite accounting for less than 8% of Earth’s land coverage, freshwater wetlands are the foremost contributor to global methane emissions. Although methane in wetlands originates from soil microbial processes, discerning the primary active microbial lineages and their metabolic roles has proven elusive. Here we sampled one of the most prolific methane-emitting wetlands in the continental United States over a five-year span and constructed a microbial genome resource of 17,333 metagenome assembled genomes. This catalog encompasses 2,502 unique genomes from 72 bacterial and archaeal phyla with more than half representing novel lineages lacking genomic representation. Integration of these wetland microbial genomes with 133 spatially and temporally resolved metatranscriptomes, along with paired amplicon, geochemical and greenhouse gas data from over 700 samples, afforded new insights into the metabolic reservoir harbored in wetland soils. We delineate the transcriptional contributions of each genome to biogeochemically relevant traits to uncover the dominant axes of environmental variation in wetland soils. Despite extended flooding captured in our sampling, soil redox shifts failed to reconfigure the transcriptional profiles of 101 methanogen and methanotroph genomes, indicating microbial methane cycling resilience to climate perturbations. Employing regression-based modeling, we identified the integrated carbon and energy assignments responsible for porewater methane hotspots, exposing the microbial metabolic circuitry that underpins wetland methane production. Our findings show how microbial-scale biogeochemical interactions within freshwater wetland soils can amplify into significant ecosystem-scale fluxes.

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

Ellenbogen¹,

Borton²,

McGivern³

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

While wetlands are major sources of biogenic methane (CH4), our understanding of resident microbial metabolisms is incomplete, which compromises 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 metabolisms, we revealed that nearly 20% (72) of the metagenome-assembled genomes (MAGs) encoded potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; for Methanosarcinales and Methanobacteriales MAGs, these data indicated use of methylated oxygen compounds (e.g., methanol), while for Methanomassiliicoccales, they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1700 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 activity. Methanogenesis across increasing permafrost thaw is thus revised from sole dominance of hydrogenotrophic production, and the appearance of acetoclastic at full thaw, to consider 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.

show abstract

Targeted curation of the gut microbial gene content modulating human cardiovascular disease

Cited by 4 publications

References 77 publications

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

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

Mapping the soil microbiome functions shaping wetland methane emissions

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

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