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

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. Cook, Ariane Briegel, Tanja Woyke, Emiley Eloe-Fadrosh, Nicole Shapiro, Scott G. Bryan, Savannah Sleezer, Joshua Dimapilis, Cristina Gonzalez, Lizett Gonzalez, Marlene Noriega, Matthias Hess, Ross P. Carlson, Lan Liu, Meng-Meng Li, Zheng-Han Lian, Siqi Zhu, Fan Liu, Xian Sun, Beile Gao, Ritesh Mewalal, Miranda Harmon-Smith, Ian K. Blaby, Jan-Fang Cheng, Peter K. Weber, Gabriela Grigorean, Wen-Jun Li, Anne E. Dekas, Jennifer Pett-Ridge, Jeremy A. Dodsworth, Marike Palmer () and Brian P. Hedlund ()
Additional contact information
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
Steffen Buessecker: Stanford University
Damon Mosier: California State University
Alise R. Muok: Sylviusweg 72
Nicole Torosian: Las Vegas
Allison M. Cook: Las Vegas
Ariane Briegel: Sylviusweg 72
Tanja Woyke: Lawrence Berkeley National Laboratory
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
Lan Liu: Sun Yat-Sen University
Meng-Meng Li: Sun Yat-Sen University
Zheng-Han Lian: Sun Yat-Sen University
Siqi Zhu: Chinese Academy of Sciences
Fan Liu: Chinese Academy of Sciences
Xian Sun: Chinese Academy of Sciences
Beile Gao: 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
Anne E. Dekas: Stanford University
Jennifer Pett-Ridge: Lawrence Livermore National Laboratory
Jeremy A. Dodsworth: California State University
Marike Palmer: Las Vegas
Brian P. Hedlund: Las Vegas

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-53784-3

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