Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

McGivern, Bridget B.; Tfaily, Malak M.; Borton, Mikayla A.; Kosina, Suzanne M.; Daly, Rebecca A.; Nicora, Carrie D.; Purvine, Samuel O.; Wong, Allison R.; Lipton, Mary S.; Hoyt, David W.; Northen, Trent R.; Hagerman, Ann E.; Wrighton, Kelly C.

doi:10.1038/s41467-021-22765-1

Title: Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

Journal Article · 28 April 2021 · Nature Communications

DOI: https://doi.org/10.1038/s41467-021-22765-1 · OSTI ID:1779988

; Tfaily, Malak M.; Borton, Mikayla A.;

; Daly, Rebecca A.;

;

; Lipton, Mary S.;

;

; Hagerman, Ann E.; Wrighton, Kelly C.

Abstract Microorganisms play vital roles in modulating organic matter decomposition and nutrient cycling in soil ecosystems. The enzyme latch paradigm posits microbial degradation of polyphenols is hindered in anoxic peat leading to polyphenol accumulation, and consequently diminished microbial activity. This model assumes that polyphenols are microbially unavailable under anoxia, a supposition that has not been thoroughly investigated in any soil type. Here, we use anoxic soil reactors amended with and without a chemically defined polyphenol to test this hypothesis, employing metabolomics and genome-resolved metaproteomics to interrogate soil microbial polyphenol metabolism. Challenging the idea that polyphenols are not bioavailable under anoxia, we provide metabolite evidence that polyphenols are depolymerized, resulting in monomer accumulation, followed by the generation of small phenolic degradation products. Further, we show that soil microbiome function is maintained, and possibly enhanced, with polyphenol addition. In summary, this study provides chemical and enzymatic evidence that some soil microbiota can degrade polyphenols under anoxia and subvert the assumed polyphenol lock on soil microbial metabolism.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

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

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; SC0018022; SC0019746

OSTI ID:: 1779988

Report Number(s):: PNNL-SA--155819; 2466; PII: 22765

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 12; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Resources and Biological Activities of Natural Polyphenols Li, An-Na; Li, Sha; Zhang, Yu-Jie Nutrients, Vol. 6, Issue 12 https://doi.org/10.3390/nu6126020	journal	December 2014
The role of L-DOPA in plants Soares, Anderson Ricardo; Marchiosi, Rogério; Siqueira-Soares, Rita de Cássia Plant Signaling & Behavior, Vol. 9, Issue 4 https://doi.org/10.4161/psb.28275	journal	March 2014
Effects of sterilization techniques on chemodenitrification and N₂O production in tropical peat soil microcosms Buessecker, Steffen; Tylor, Kaitlyn; Nye, Joshua Biogeosciences, Vol. 16, Issue 23 https://doi.org/10.5194/bg-16-4601-2019	journal	January 2019
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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