Microbial polyphenol metabolism is part of the thawing permafrost carbon cycle

McGivern, Bridget B.; Cronin, Dylan R.; Ellenbogen, Jared B.; Borton, Mikayla A.; Knutson, Eleanor L.; Freire-Zapata, Viviana; Bouranis, John A.; Bernhardt, Lukas; Hernandez, Alma I.; Flynn, Rory M.; Woyda, Reed; Cory, Alexandra B.; Wilson, Rachel M.; Chanton, Jeffrey P.; Woodcroft, Ben J.; Ernakovich, Jessica G.; Tfaily, Malak M.; Sullivan, Matthew B.; Tyson, Gene W.; Rich, Virginia I.; Hagerman, Ann E.; Wrighton, Kelly C.

doi:10.1038/s41564-024-01691-0

Microbial polyphenol metabolism is part of the thawing permafrost carbon cycle

Journal Article · Tue May 28 00:00:00 EDT 2024 · Nature Microbiology

DOI:https://doi.org/10.1038/s41564-024-01691-0· OSTI ID:2367421

; Cronin, Dylan R.; Ellenbogen, Jared B.; ; Knutson, Eleanor L.; ; Bouranis, John A.; Bernhardt, Lukas; Hernandez, Alma I.; Flynn, Rory M.; Woyda, Reed; Cory, Alexandra B.; Wilson, Rachel M.; Chanton, Jeffrey P.; ; ; Tfaily, Malak M.; ; ; Rich, Virginia I. more »

Abstract

With rising global temperatures, permafrost carbon stores are vulnerable to microbial degradation. The enzyme latch theory states that polyphenols should accumulate in saturated peatlands due to diminished phenol oxidase activity, inhibiting resident microbes and promoting carbon stabilization. Pairing microbiome and geochemical measurements along a permafrost thaw-induced saturation gradient in Stordalen Mire, a model Arctic peatland, we confirmed a negative relationship between phenol oxidase expression and saturation but failed to support other trends predicted by the enzyme latch. To inventory alternative polyphenol removal strategies, we built CAMPER, a gene annotation tool leveraging polyphenol enzyme knowledge gleaned across microbial ecosystems. Applying CAMPER to genome-resolved metatranscriptomes, we identified genes for diverse polyphenol-active enzymes expressed by various microbial lineages under a range of redox conditions. This shifts the paradigm that polyphenols stabilize carbon in saturated soils and highlights the need to consider both oxic and anoxic polyphenol metabolisms to understand carbon cycling in changing ecosystems.

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Research Organization:: Battelle Memorial Institute, Columbus, OH (United States); Colorado State Univ., Fort Collins, CO (United States); Univ. of Arizona, Tucson, AZ (United States); Univ. of California, Oakland, CA (United States); Univ. of Colorado, Boulder, CO (United States); Univ. of New Hampshire, Durham, NH (United States)

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

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0004632; SC0010580; SC0019746; SC0021350; SC0023084; SC0023456

OSTI ID:: 2367421

Alternate ID(s):: OSTI ID: 2472177
OSTI ID: 3012456

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 6 Vol. 9; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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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

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