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Genome-guided isolation of the hyperthermophilic aerobe Fervidibacter sacchari reveals conserved polysaccharide metabolism in the Armatimonadota

Author

Listed:
  • Nancy O. Nou

    (Las Vegas)

  • Jonathan K. Covington

    (Las Vegas)

  • Dengxun Lai

    (Las Vegas)

  • Xavier Mayali

    (Lawrence Livermore National Laboratory)

  • Cale O. Seymour

    (Las Vegas)

  • Juliet Johnston

    (Lawrence Livermore National Laboratory)

  • Jian-Yu Jiao

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Steffen Buessecker

    (Stanford University)

  • Damon Mosier

    (California State University
    University of Calgary)

  • Alise R. Muok

    (Sylviusweg 72)

  • Nicole Torosian

    (Las Vegas)

  • Allison M. Cook

    (Las Vegas)

  • Ariane Briegel

    (Sylviusweg 72)

  • Tanja Woyke

    (Lawrence Berkeley National Laboratory
    Life and Environmental Sciences)

  • Emiley Eloe-Fadrosh

    (Lawrence Berkeley National Laboratory)

  • Nicole Shapiro

    (Lawrence Berkeley National Laboratory)

  • Scott G. Bryan

    (Las Vegas)

  • Savannah Sleezer

    (Las Vegas)

  • Joshua Dimapilis

    (California State University)

  • Cristina Gonzalez

    (California State University)

  • Lizett Gonzalez

    (California State University)

  • Marlene Noriega

    (California State University)

  • Matthias Hess

    (University of California Davis)

  • Ross P. Carlson

    (Montana State University
    Montana State University)

  • Lan Liu

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Meng-Meng Li

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Zheng-Han Lian

    (Sun Yat-Sen University
    Sun Yat-Sen University)

  • Siqi Zhu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Fan Liu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Xian Sun

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Beile Gao

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Ritesh Mewalal

    (Lawrence Berkeley National Laboratory)

  • Miranda Harmon-Smith

    (Lawrence Berkeley National Laboratory)

  • Ian K. Blaby

    (Lawrence Berkeley National Laboratory)

  • Jan-Fang Cheng

    (Lawrence Berkeley National Laboratory)

  • Peter K. Weber

    (Lawrence Livermore National Laboratory)

  • Gabriela Grigorean

    (University of California Davis)

  • Wen-Jun Li

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Chinese Academy of Sciences)

  • Anne E. Dekas

    (Stanford University)

  • Jennifer Pett-Ridge

    (Lawrence Livermore National Laboratory)

  • Jeremy A. Dodsworth

    (California State University)

  • Marike Palmer

    (Las Vegas
    University of Manitoba)

  • Brian P. Hedlund

    (Las Vegas
    University of Nevada Las Vegas)

Abstract

Few aerobic hyperthermophilic microorganisms degrade polysaccharides. Here, we describe the genome-enabled enrichment and optical tweezer-based isolation of an aerobic polysaccharide-degrading hyperthermophile, Fervidibacter sacchari, previously ascribed to candidate phylum Fervidibacteria. F. sacchari uses polysaccharides and monosaccharides for growth at 65–87.5 °C and expresses 191 carbohydrate-active enzymes (CAZymes) according to RNA-Seq and proteomics, including 31 with unusual glycoside hydrolase domains (GH109, GH177, GH179). Fluorescence in-situ hybridization and nanoscale secondary ion mass spectrometry confirmed rapid assimilation of 13C-starch in spring sediments. Purified GHs were optimally active at 80–100 °C on ten different polysaccharides. Finally, we propose reassigning Fervidibacteria as a class within phylum Armatimonadota, along with 18 other species, and show that a high number and diversity of CAZymes is a hallmark of the phylum, in both aerobic and anaerobic lineages. Our study establishes Fervidibacteria as hyperthermophilic polysaccharide degraders in terrestrial geothermal springs and suggests a broad role for Armatimonadota in polysaccharide catabolism.

Suggested Citation

  • Nancy O. Nou & Jonathan K. Covington & Dengxun Lai & Xavier Mayali & Cale O. Seymour & Juliet Johnston & Jian-Yu Jiao & Steffen Buessecker & Damon Mosier & Alise R. Muok & Nicole Torosian & Allison M., 2024. "Genome-guided isolation of the hyperthermophilic aerobe Fervidibacter sacchari reveals conserved polysaccharide metabolism in the Armatimonadota," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53784-3
    DOI: 10.1038/s41467-024-53784-3
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    References listed on IDEAS

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    1. Steffen Buessecker & Marike Palmer & Dengxun Lai & Joshua Dimapilis & Xavier Mayali & Damon Mosier & Jian-Yu Jiao & Daniel R. Colman & Lisa M. Keller & Emily St. John & Michelle Miranda & Cristina Gon, 2022. "An essential role for tungsten in the ecology and evolution of a previously uncultivated lineage of anaerobic, thermophilic Archaea," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Christian Rinke & Patrick Schwientek & Alexander Sczyrba & Natalia N. Ivanova & Iain J. Anderson & Jan-Fang Cheng & Aaron Darling & Stephanie Malfatti & Brandon K. Swan & Esther A. Gies & Jeremy A. Do, 2013. "Insights into the phylogeny and coding potential of microbial dark matter," Nature, Nature, vol. 499(7459), pages 431-437, July.
    3. Peter Menzel & Kim Lee Ng & Anders Krogh, 2016. "Fast and sensitive taxonomic classification for metagenomics with Kaiju," Nature Communications, Nature, vol. 7(1), pages 1-9, September.
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