Microbiome–metabolite linkages drive greenhouse gas dynamics over a permafrost thaw gradient

Freire-Zapata, Viviana; Holland-Moritz, Hannah; Cronin, Dylan R.; Aroney, Sam; Smith, Derek A.; Wilson, Rachel M.; Ernakovich, Jessica G.; Woodcroft, Benjamin J.; Bagby, Sarah C.; Hodgkins, Suzanne B.; Mondav, Rhiannon; E. Cross, Jennifer; Fahnestock, Maria Florencia; Ferriere, Regis; Ibba, Michael; Saleska, Scott R.; Varner, Ruth K.; Zayed, Ahmed A.; Rich, Virginia I.; Sullivan, Matthew B.; Stegen, James C.; Tfaily, Malak M.

doi:10.1038/s41564-024-01800-z

Title: Microbiome–metabolite linkages drive greenhouse gas dynamics over a permafrost thaw gradient

Journal Article · 01 October 2024 · Nature Microbiology

DOI: https://doi.org/10.1038/s41564-024-01800-z · OSTI ID:2452820

^[1]; Holland-Moritz, Hannah ^[2]; Cronin, Dylan R. ^[3];

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^[5]; Hodgkins, Suzanne B. ^[3]; Mondav, Rhiannon ^[7]; E. Cross, Jennifer ^[8]; Fahnestock, Maria Florencia ^[2]; Ferriere, Regis ^[1]; Ibba, Michael ^[9];

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^[2]; Zayed, Ahmed A. ^[3]; Rich, Virginia I. ^[3];

^[3] more »

Univ. of Arizona, Tucson, AZ (United States)
Univ. of New Hampshire, Durham, NH (United States)
The Ohio State Univ., Columbus, OH (United States)
Queensland University of Technology (Australia)
Case Western Reserve Univ., Cleveland, OH (United States)
Florida State Univ., Tallahassee, FL (United States)
Lund Univ. (Sweden)
Colorado State Univ., Fort Collins, CO (United States)
Chapman Univ., Orange, CA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Washington State Univ., Pullman, WA (United States)

Interactions between microbiomes and metabolites play crucial roles in the environment, yet how these interactions drive greenhouse gas emissions during ecosystem changes remains unclear. Here we analysed microbial and metabolite composition across a permafrost thaw gradient in Stordalen Mire, Sweden, using paired genome-resolved metagenomics and high-resolution Fourier transform ion cyclotron resonance mass spectrometry guided by principles from community assembly theory to test whether microorganisms and metabolites show concordant responses to changing drivers. Our analysis revealed divergence between the inferred microbial versus metabolite assembly processes, suggesting distinct responses to the same selective pressures. This contradicts common assumptions in trait-based microbial models and highlights the limitations of measuring microbial community-level data alone. Furthermore, feature-scale analysis revealed connections between microbial taxa, metabolites and observed CO₂ and CH₄ porewater variations. Our study showcases insights gained by using feature-level data and microorganism–metabolite interactions to better understand metabolic processes that drive greenhouse gas emissions during ecosystem changes.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

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

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0021349

OSTI ID:: 2452820

Report Number(s):: PNNL-SA--196799

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 11 Vol. 9; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Controls on Soil Organic Matter Degradation and Subsequent Greenhouse Gas Emissions Across a Permafrost Thaw Gradient in Northern Sweden AminiTabrizi, Roya; Wilson, Rachel M.; Fudyma, Jane D. Frontiers in Earth Science, Vol. 8 https://doi.org/10.3389/feart.2020.557961	journal	September 2020
Sulfate-reducing microorganisms in wetlands – fameless actors in carbon cycling and climate change Pester, Michael Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00072	journal	January 2012
Estimating and mapping ecological processes influencing microbial community assembly Stegen, James C.; Lin, Xueju; Fredrickson, Jim K. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00370	journal	May 2015
Coupling Spatiotemporal Community Assembly Processes to Changes in Microbial Metabolism Graham, Emily B.; Crump, Alex R.; Resch, Charles T. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01949	journal	December 2016
Biotic and Environmental Drivers of Plant Microbiomes Across a Permafrost Thaw Gradient Hough, Moira; McClure, Amelia; Bolduc, Benjamin Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.00796	journal	May 2020
The Transition From Stochastic to Deterministic Bacterial Community Assembly During Permafrost Thaw Succession Doherty, Stacey Jarvis; Barbato, Robyn A.; Grandy, A. Stuart Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.596589	journal	November 2020
Inferring the Contribution of Microbial Taxa and Organic Matter Molecular Formulas to Ecological Assembly Danczak, Robert E.; Sengupta, Aditi; Fansler, Sarah J. Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.803420	journal	February 2022
Coupled Biotic-Abiotic Processes Control Biogeochemical Cycling of Dissolved Organic Matter in the Columbia River Hyporheic Zone Fudyma, Jane D.; Chu, Rosalie K.; Graf Grachet, Nathalia Frontiers in Water, Vol. 2 https://doi.org/10.3389/frwa.2020.574692	journal	January 2021
Metagenome-assembled genomes (MAGs) from Stordalen Mire, Sweden Cronin, Dylan; Institute, NSF EMERGE Biology Integration Zenodo https://doi.org/10.5281/zenodo.10426238	dataset	January 2023
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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