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Decrypting bacterial polyphenol metabolism in an anoxic wetland soil

Author

Listed:
  • 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)

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.

Suggested Citation

  • 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. Nor, 2021. "Decrypting bacterial polyphenol metabolism in an anoxic wetland soil," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-22765-1
    DOI: 10.1038/s41467-021-22765-1
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    Cited by:

    1. Nicholas O. E. Ofiti & Michael W. I. Schmidt & Samuel Abiven & Paul J. Hanson & Colleen M. Iversen & Rachel M. Wilson & Joel E. Kostka & Guido L. B. Wiesenberg & Avni Malhotra, 2023. "Climate warming and elevated CO2 alter peatland soil carbon sources and stability," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. Payal Chirania & Evert K. Holwerda & Richard J. Giannone & Xiaoyu Liang & Suresh Poudel & Joseph C. Ellis & Yannick J. Bomble & Robert L. Hettich & Lee R. Lynd, 2022. "Metaproteomics reveals enzymatic strategies deployed by anaerobic microbiomes to maintain lignocellulose deconstruction at high solids," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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