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

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 <sup>13</sup>C-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.

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Publication Details

Journal
Nature Communications
Published
2024-11-04
DOI
https://doi.org/10.1038/s41467-024-53784-3
Citations
9
Primary Topic
Microbial Community Ecology and Physiology
Type
article
Field-Weighted Citation Impact
4.13

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article

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

Anne Dekas, Jennifer Pett‐Ridge, Dengxun Lai, Damon Mosier et al.
9 citations
Nature Communications
Microbial Community Ecology and Physiology
4.13
article

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

Anne Dekas, Jennifer Pett‐Ridge, Dengxun Lai, Damon Mosier, Tanja Woyke, Ross P. Carlson, Miranda Harmon‐Smith, Xian Sun, Ritesh Mewalal, Jan‐Fang Cheng, Scott G. Bryan, Nicole Shapiro, Peter Weber, Ariane Briegel, Marlene Noriega, Brian P. Hedlund, Gabriela Grigorean, Siqi Zhu, Matthias Hess, Ian K. Blaby, Nancy O. Nou, Jeremy A. Dodsworth, Lizett Gonzalez, Steffen Buessecker, Xavier Mayali, Emiley A. Eloe‐Fadrosh, Marike Palmer, Beile Gao, Cale O. Seymour, Alise R. Muok, Allison M. Cook, Juliet Johnston, Jian‐Yu Jiao, Jonathan K. Covington, Zheng‐Han Lian, Joshua Dimapilis, Nicole Torosian, Savannah Sleezer, Wen‐Jun Li, Lan Liu, Cristina González, Fan Liu, Meng‐Meng Li
article en
9 citations

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 <sup>13</sup>C-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.

Nature CommunicationsVol. 15(1)
Leiden University (NL), Lawrence Livermore National Laboratory (US), University of Nevada, Las Vegas (US), Lawrence Berkeley National Laboratory (US), University of California, Merced (US), Sun Yat-sen University (CN), University of Calgary (CA), Joint Genome Institute (US), Chinese Academy of Sciences (CN), Montana State University (US), Institute of Oceanology (CN), Xinjiang Institute of Ecology and Geography (CN), South China Sea Institute Of Oceanology (CN), Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (CN), University of Chinese Academy of Sciences (CN), California State University, San Bernardino (US), University of Manitoba (CA), University of California, Davis (US), Stanford University (US)
National Science Foundation, U.S. Department of Energy, National Aeronautics and Space Administration, Nevada Space Grant Consortium, Joint Genome Institute, National Natural Science Foundation of China, Nuclear Safety and Security Commission, National Institutes of Health, Office of Science, National Institute of General Medical Sciences, Lawrence Livermore National Laboratory
Openalex Percentile: Top 6%
Microbial Community Ecology and Physiology
4.13
DOIOpen Access PDFOpenAlex
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