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

• Published in: Nature communications 2024-11, Vol.15 (1)
• Main Authors: Nou, Nancy O., Covington, Jonathan K., Lai, Dengxun, Mayali, Xavier, Seymour, Cale O., Johnston, Juliet, Jiao, Jian-Yu, Buessecker, Steffen, Mosier, Damon, Muok, Alise R., Torosian, Nicole, Cook, Allison M., Briegel, Ariane, Woyke, Tanja, Eloe-Fadrosh, Emiley, Shapiro, Nicole, Bryan, Scott G., Sleezer, Savannah, Dimapilis, Joshua, Gonzalez, Cristina, Gonzalez, Lizett, Noriega, Marlene, Hess, Matthias, Carlson, Ross P., Liu, Lan, Li, Meng-Meng, Lian, Zheng-Han, Zhu, Siqi, Liu, Fan, Sun, Xian, Gao, Beile, Mewalal, Ritesh, Harmon-Smith, Miranda, Blaby, Ian K., Cheng, Jan-Fang, Weber, Peter K., Grigorean, Gabriela, Li, Wen-Jun, Dekas, Anne E., Pett-Ridge, Jennifer, Dodsworth, Jeremy A., Palmer, Marike, Hedlund, Brian P.
• Format: Article
• Language: English
• Subjects: bacterial physiology; Biological and medical sciences; environmental microbiology; microbial ecology; polysaccharides
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-53784-3

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.