Nature Communications (Nov 2024)

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,
  • Brian P. Hedlund

DOI
https://doi.org/10.1038/s41467-024-53784-3
Journal volume & issue
Vol. 15, no. 1
pp. 1 – 17

Abstract

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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.