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Peer-reviewedCC BYmSystems

Mapping the soil microbiome functions shaping wetland methane emissions

11 more authors
13 affiliations
  1. 1Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO, 80521
  2. 2Department of Biology, Syracuse University, Syracuse, NY, 13210
  3. 3School of Geosciences, University of Louisiana at Lafayette, Lafayette, LA 70503
  4. 4Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, St. Lucia, QLD, Australia
  5. 5Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, 99352
  6. 6Center for Pan-third Pole Environment, Lanzhou University, Lanzhou 730000, China
  7. 7Department of Microbiology, The Ohio State University, Columbus, OH 43210
  8. 8Data Science and Learning, Argonne National Laboratory, Lemont, IL 60439
  9. 9DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720
  10. 10Lawrence Berkeley National Lab, Berkeley, CA, 94720
  11. 11Department of Integrative Biology, University of Colorado Denver, Denver, CO, 80217
  12. 12Department of Environmental Resources Engineering, State University of New York College of Environmental Sciences and Forestry, Syracuse, New York, 13210
  13. 13Department of Civil, Environmental & Geodetic Engineering, The Ohio State University, Columbus, OH, 43210

Abstract

Accounting for only 8% of Earth’s land cover, freshwater wetlands remain the foremost contributors to global methane emissions. Yet the microorganisms and processes underlying methane emissions from wetland soils remain poorly understood. Over a five-year period, we surveyed the microbial membership and in situ methane measurements from over 700 samples in one of the most prolific methane-emitting wetlands in the United States. We constructed a catalog of 2,502 metagenome-assembled genomes (MAGs), with more than half of the 70 bacterial and archaeal phyla sampled containing novel lineages. Integration of these data with 133 soil metatranscriptomes provided a genome-resolved view of the biogeochemical specialization and versatility expressed over wetland soil spatial and temporal gradients. Centimeter-scale depth differences best explained patterns of microbial community structure and transcribed functionalities, even more than land cover or temporal information. Moreover, while extended flooding restructured soil redox, this perturbation failed to reconfigure the transcriptional profiles of methane-cycling microorganisms, contrasting with theoretically expected responses to hydrological perturbations. Co-expression analyses, coupled with depth-resolved methane measurements, revealed the metabolisms and trophic structures most predictive of methane hotspots. Mapping the spatiotemporal transcriptional patterns on this compendium of biogeochemically classified soil-derived genomes begins to untangle the microbial carbon, energy, and nutrient processing contributing to wetland methane production. IMPORTANCE Soil microbial ecology is increasingly recognized as essential to climate mitigation, but realizing its full potential requires shifting from static genome inventories to dynamic assessments of microbial activity. This study shows that methane-cycling microbes exhibit stable, depth-stratified expression patterns, even in response to major redox and flooding shifts, undermining assumptions that water-table manipulations common in wetland management can alone reduce methanogenesis. Instead, methane cycling is shaped by spatially organized, transcriptionally active networks involving not only methanogens but also methanotrophs, fermenters, and iron reducers. These findings expose the limitations of genome-only models and highlight the need for soil diagnostics that capture in situ activity. Together, we provide a foundation for developing activity-based microbiome tools, embedding microbial functions into Earth system models, and designing interventions that move beyond “single-lever” strategies and instead work with the structure and dynamics of microbial communities as complex, layered systems.

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BibTeX
@article{borton2026mapping,
  title = {{Mapping the soil microbiome functions shaping wetland methane emissions}},
  author = {Mikayla A. Borton and Angela Oliverio and Adrienne B. Narrowe and Jorge A. Villa and Christian Rinke and David W. Hoyt and Pengfei Liu and Bridget B. McGivern and Emily K. Bechtold and Jared Ellenbogen and Rebecca A. Daly and Garrett J. Smith and Jordan C. Angle and Rory M. Flynn and Andrew Freiburger and Katherine Louie and Brooke Stemple and Trent R. Northen and Christopher Henry and Christopher S. Miller and Timothy Morin and Gil Bohrer and Kelly C. Wrighton},
  journal = {mSystems},
  year = {2026},
  month = jun,
  doi = {10.1128/msystems.00680-25},
  url = {https://doi.org/10.1128/msystems.00680-25},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Mapping the soil microbiome functions shaping wetland methane emissions
AU  - Mikayla A. Borton
AU  - Angela Oliverio
AU  - Adrienne B. Narrowe
AU  - Jorge A. Villa
AU  - Christian Rinke
AU  - David W. Hoyt
AU  - Pengfei Liu
AU  - Bridget B. McGivern
AU  - Emily K. Bechtold
AU  - Jared Ellenbogen
AU  - Rebecca A. Daly
AU  - Garrett J. Smith
AU  - Jordan C. Angle
AU  - Rory M. Flynn
AU  - Andrew Freiburger
AU  - Katherine Louie
AU  - Brooke Stemple
AU  - Trent R. Northen
AU  - Christopher Henry
AU  - Christopher S. Miller
AU  - Timothy Morin
AU  - Gil Bohrer
AU  - Kelly C. Wrighton
PY  - 2026
DA  - 2026/06/01
JO  - mSystems
DO  - 10.1128/msystems.00680-25
UR  - https://doi.org/10.1128/msystems.00680-25
AB  - Accounting for only 8% of Earth’s land cover, freshwater wetlands remain the foremost contributors to global methane emissions. Yet the microorganisms and processes underlying methane emissions from wetland soils remain poorly understood. Over a five-year period, we surveyed the microbial membership and in situ methane measurements from over 700 samples in one of the most prolific methane-emitting wetlands in the United States. We constructed a catalog of 2,502 metagenome-assembled genomes (MAGs), with more than half of the 70 bacterial and archaeal phyla sampled containing novel lineages. Integration of these data with 133 soil metatranscriptomes provided a genome-resolved view of the biogeochemical specialization and versatility expressed over wetland soil spatial and temporal gradients. Centimeter-scale depth differences best explained patterns of microbial community structure and transcribed functionalities, even more than land cover or temporal information. Moreover, while extended flooding restructured soil redox, this perturbation failed to reconfigure the transcriptional profiles of methane-cycling microorganisms, contrasting with theoretically expected responses to hydrological perturbations. Co-expression analyses, coupled with depth-resolved methane measurements, revealed the metabolisms and trophic structures most predictive of methane hotspots. Mapping the spatiotemporal transcriptional patterns on this compendium of biogeochemically classified soil-derived genomes begins to untangle the microbial carbon, energy, and nutrient processing contributing to wetland methane production. IMPORTANCE Soil microbial ecology is increasingly recognized as essential to climate mitigation, but realizing its full potential requires shifting from static genome inventories to dynamic assessments of microbial activity. This study shows that methane-cycling microbes exhibit stable, depth-stratified expression patterns, even in response to major redox and flooding shifts, undermining assumptions that water-table manipulations common in wetland management can alone reduce methanogenesis. Instead, methane cycling is shaped by spatially organized, transcriptionally active networks involving not only methanogens but also methanotrophs, fermenters, and iron reducers. These findings expose the limitations of genome-only models and highlight the need for soil diagnostics that capture in situ activity. Together, we provide a foundation for developing activity-based microbiome tools, embedding microbial functions into Earth system models, and designing interventions that move beyond “single-lever” strategies and instead work with the structure and dynamics of microbial communities as complex, layered systems.
SN  - 2379-5077
ER  -