Genome-Guided Isolation of the Hyperthermophilic Aerobe Fervidibacter sacchari Reveals Conserved Polysaccharide Metabolism in the Armatimonadota

Authors

• Nancy O. Nou, University of Nevada, Las Vegas
• Jonathan K. Covington, University of Nevada, Las Vegas
• Dengxun Lai, University of Nevada, Las Vegas
• Xavier Mayali, Lawrence Livermore National LaboratoryFollow
• Cale O. Seymour, University of Nevada, Las Vegas
• Juliet Johnston, Lawrence Livermore National Laboratory
• Jian-Yu Jiao, Sun Yat-sen University
• Steffen Buessecker, Stanford UniversityFollow
• Damon Mosier, University of Calgary
• Alise R. Muok, Leiden University
• Nicole Torosian, University of Nevada, Las Vegas
• Allison M. Cook, University of Nevada, Las Vegas
• Ariane Briegel, Leiden University
• Tanja Woyke, University of California, MercedFollow
• Emiley Eloe-Fadrosh, Lawrence Berkeley National LaboratoryFollow
• Nicole Shapiro, Lawrence Berkeley National Laboratory
• Scott G. Bryan, University of Nevada, Las Vegas
• Savannah Sleezer, University of Nevada, Las Vegas
• Joshua Dimapilis, California State University - San Bernardino
• Cristina Gonzalez, California State University - San Bernardino
• Lizett Gonzalez, California State University - San Bernardino
• Marlene Noriega, California State University - San Bernardino
• Matthias Hess, University of California, DavisFollow
• Ross P. Carlson, Montana State University-BozemanFollow
• Lan Liu, Sun Yat-Sen University
• Meng-Meng Li, Sun Yat-sen University
• Zheng-Han Lian, Sun Yat-sen University
• Siqii 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 E. Pett-Ridge, Lawrence Livermore National Laboratory
• Jeremy A. Dodsworth, California State University - San Bernardino
• Marike Palmer, University of Nevada, Las Vegas
• Brian P. Hedlund, University of Nevada, Las VegasFollow

Document Type

Article

Publication Date

11-4-2024

Publication Title

Nature Communications

Volume

15

First page number:

1

Last page number:

17

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.

Controlled Subject

Microorganisms; Polysaccharides--Structure; Microbial biotechnology

Disciplines

Microbial Physiology | Molecular Biology

File Format

PDF

File Size

2900 KB

Language

English

Rights

IN COPYRIGHT. For more information about this rights statement, please visit http://rightsstatements.org/vocab/InC/1.0/

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Repository Citation

Nou, N. O., Covington, J. K., Lai, D., Mayali, X., Seymour, C. O., Johnston, J., Jiao, J., Buessecker, S., Mosier, D., Muok, A. R., Torosian, N., Cook, A. M., Briegel, A., Woyke, T., Eloe-Fadrosh, E., Shapiro, N., Bryan, S. G., Sleezer, S., Dimapilis, J., Gonzalez, C., Gonzalez, L., Noriega, M., Hess, M., Carlson, R. P., Liu, L., Li, M., Lian, Z., Zhu, S., Liu, F., Sun, X., Gao, B., Mewalal, R., Harmon-Smith, M., Blaby, I. K., Cheng, J., Weber, P. K., Grigorean, G., Li, W., Dekas, A. E., Pett-Ridge, J. E., Dodsworth, J. A., Palmer, M., Hedlund, B. P. (2024). Genome-Guided Isolation of the Hyperthermophilic Aerobe Fervidibacter sacchari Reveals Conserved Polysaccharide Metabolism in the Armatimonadota. Nature Communications, 15 1-17.
http://dx.doi.org/10.1038/s41467-024-53784-3