Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

Bridget B. McGivern, Malak M. Tfaily, Mikayla A. Borton, Suzanne M. Kosina, Rebecca A. Daly, Carrie D. Nicora, Samuel O. Purvine, Allison R. Wong, Mary S. Lipton, David W. Hoyt, Trent R. Northen, Ann E. Hagerman and Kelly C. Wrighton ()
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Bridget B. McGivern: Colorado State University
Malak M. Tfaily: University of Arizona
Mikayla A. Borton: Colorado State University
Suzanne M. Kosina: Lawrence Berkeley National Laboratory
Rebecca A. Daly: Colorado State University
Carrie D. Nicora: Pacific Northwest National Laboratory
Samuel O. Purvine: Pacific Northwest National Laboratory
Allison R. Wong: Pacific Northwest National Laboratory
Mary S. Lipton: Lawrence Berkeley National Laboratory
David W. Hoyt: Pacific Northwest National Laboratory
Trent R. Northen: University of Arizona
Ann E. Hagerman: Miami University
Kelly C. Wrighton: Colorado State University

Nature Communications, 2021, vol. 12, issue 1, 1-16

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-22765-1

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