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
Affiliations
- Nancy O. Nou
- School of Life Sciences, University of Nevada, Las Vegas
- Jonathan K. Covington
- School of Life Sciences, University of Nevada, Las Vegas
- Dengxun Lai
- School of Life Sciences, University of Nevada, Las Vegas
- Xavier Mayali
- Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory
- Cale O. Seymour
- School of Life Sciences, University of Nevada, Las Vegas
- Juliet Johnston
- Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory
- Jian-Yu Jiao
- State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory, Sun Yat-Sen University
- Steffen Buessecker
- Department of Earth System Science, Stanford University
- Damon Mosier
- Department of Biology, California State University
- Alise R. Muok
- Department of Microbial Sciences, Institute of Biology, Leiden University, Sylviusweg 72
- Nicole Torosian
- School of Life Sciences, University of Nevada, Las Vegas
- Allison M. Cook
- School of Life Sciences, University of Nevada, Las Vegas
- Ariane Briegel
- Department of Microbial Sciences, Institute of Biology, Leiden University, Sylviusweg 72
- Tanja Woyke
- DOE Joint Genome Institute, Lawrence Berkeley National Laboratory
- Emiley Eloe-Fadrosh
- DOE Joint Genome Institute, Lawrence Berkeley National Laboratory
- Nicole Shapiro
- DOE Joint Genome Institute, Lawrence Berkeley National Laboratory
- Scott G. Bryan
- School of Life Sciences, University of Nevada, Las Vegas
- Savannah Sleezer
- School of Life Sciences, University of Nevada, Las Vegas
- Joshua Dimapilis
- Department of Biology, California State University
- Cristina Gonzalez
- Department of Biology, California State University
- Lizett Gonzalez
- Department of Biology, California State University
- Marlene Noriega
- Department of Biology, California State University
- Matthias Hess
- Department of Animal Science, University of California Davis
- Ross P. Carlson
- Chemical and Biological Engineering, Montana State University
- Lan Liu
- State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory, Sun Yat-Sen University
- Meng-Meng Li
- State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory, Sun Yat-Sen University
- Zheng-Han Lian
- State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory, Sun Yat-Sen University
- Siqi Zhu
- CAS Key Laboratory of Tropical Marine Bio Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences
- Fan Liu
- CAS Key Laboratory of Tropical Marine Bio Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences
- Xian Sun
- CAS Key Laboratory of Tropical Marine Bio Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences
- Beile Gao
- CAS Key Laboratory of Tropical Marine Bio Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences
- Ritesh Mewalal
- DOE Joint Genome Institute, Lawrence Berkeley National Laboratory
- Miranda Harmon-Smith
- DOE Joint Genome Institute, Lawrence Berkeley National Laboratory
- Ian K. Blaby
- DOE Joint Genome Institute, Lawrence Berkeley National Laboratory
- Jan-Fang Cheng
- DOE Joint Genome Institute, Lawrence Berkeley National Laboratory
- Peter K. Weber
- Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory
- Gabriela Grigorean
- Proteomics Core, University of California Davis
- Wen-Jun Li
- State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory, Sun Yat-Sen University
- Anne E. Dekas
- Department of Earth System Science, Stanford University
- Jennifer Pett-Ridge
- Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory
- Jeremy A. Dodsworth
- Department of Biology, California State University
- Marike Palmer
- School of Life Sciences, University of Nevada, Las Vegas
- Brian P. Hedlund
- School of Life Sciences, University of Nevada, Las Vegas
- DOI
- https://doi.org/10.1038/s41467-024-53784-3
- Journal volume & issue
-
Vol. 15,
no. 1
pp. 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.
