Whither the genus Caldicellulosiruptor and the order Thermoanaerobacterales: phylogeny, taxonomy, ecology, and phenotype

Bing, Ryan G.; Willard, Daniel J.; Crosby, James R.; Adams, Michael W. W.; Kelly, Robert M.

doi:10.3389/fmicb.2023.1212538

Whither the genus Caldicellulosiruptor and the order Thermoanaerobacterales: phylogeny, taxonomy, ecology, and phenotype

Journal Article · Thu Aug 03 00:00:00 EDT 2023 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2023.1212538· OSTI ID:2422502

Bing, Ryan G. ^[1]; Willard, Daniel J. ^[2]; Crosby, James R. ^[2]; Adams, Michael W. W. ^[3]; Kelly, Robert M. ^[2]

North Carolina State University, Raleigh, NC (United States); North Carolina State Univ., Raleigh, NC (United States)
North Carolina State University, Raleigh, NC (United States)
Univ. of Georgia, Athens, GA (United States)

The order Thermoanaerobacterales currently consists of fermentative anaerobic bacteria, including the genus Caldicellulosiruptor. Caldicellulosiruptor are represented by thirteen species; all, but one, have closed genome sequences. Interest in these extreme thermophiles has been motivated not only by their high optimal growth temperatures (≥70°C), but also by their ability to hydrolyze polysaccharides including, for some species, both xylan and microcrystalline cellulose. Caldicellulosiruptor species have been isolated from geographically diverse thermal terrestrial environments located in New Zealand, China, Russia, Iceland and North America. Evidence of their presence in other terrestrial locations is apparent from metagenomic signatures, including volcanic ash in permafrost. Here, phylogeny and taxonomy of the genus Caldicellulosiruptor was re-examined in light of new genome sequences. Based on genome analysis of 15 strains, a new order, Caldicellulosiruptorales, is proposed containing the family Caldicellulosiruptoraceae, consisting of two genera, Caldicellulosiruptor and Anaerocellum. Furthermore, the order Thermoanaerobacterales also was re-assessed, using 91 genome-sequenced strains, and should now include the family Thermoanaerobacteraceae containing the genera Thermoanaerobacter, Thermoanaerobacterium, Caldanaerobacter, the family Caldanaerobiaceae containing the genus Caldanaerobius, and the family Calorimonaceae containing the genus Calorimonas. A main outcome of ANI/AAI analysis indicates the need to reclassify several previously designated species in the Thermoanaerobacterales and Caldicellulosiruptorales by condensing them into strains of single species. Comparative genomics of carbohydrate-active enzyme inventories suggested differentiating phenotypic features, even among strains of the same species, reflecting available nutrients and ecological roles in their native biotopes.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDoEd

Grant/Contract Number:: SC0019391; SC0022192

OSTI ID:: 2422502

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 14; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Characterization of a biogas-producing microbial community by short-read next generation DNA sequencing Wirth, Roland; Kovács, Etelka; Maróti, Gergely Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-41	journal	January 2012
Single-step ethanol production from lignocellulose using novel extremely thermophilic bacteria Svetlitchnyi, Vitali A.; Kensch, Oliver; Falkenhan, Doris A. Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-31	journal	January 2013
Microbial diversity and community composition of caecal microbiota in commercial and indigenous Indian chickens determined using 16s rDNA amplicon sequencing Pandit, Ramesh J.; Hinsu, Ankit T.; Patel, Namrata V. Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0501-9	journal	June 2018
Diversity of Thermophilic Anaerobes Wagner, Isaac D.; Wiegel, Juergen Annals of the New York Academy of Sciences, Vol. 1125, Issue 1 https://doi.org/10.1196/annals.1419.029	journal	March 2008
Comparative Analysis of Bacterial and Archaeal Communities in Methanogenic Sludge Granules from Upflow Anaerobic Sludge Blanket Reactors Treating Various Food-Processing, High-Strength Organic Wastewaters Narihiro, Takashi; Terada, Takeshi; Kikuchi, Kae Microbes and Environments, Vol. 24, Issue 2 https://doi.org/10.1264/jsme2.ME08561	journal	January 2009
Nitrogen Fixation in Thermophilic Chemosynthetic Microbial Communities Depending on Hydrogen, Sulfate, and Carbon Dioxide Nishihara, Arisa; Haruta, Shin; McGlynn, Shawn E. Microbes and Environments, Vol. 33, Issue 1 https://doi.org/10.1264/jsme2.ME17134	journal	January 2018
Nitrogen-fixing Ability and Nitrogen Fixation-related Genes of Thermophilic Fermentative Bacteria in the Genus Caldicellulosiruptor Chen, Yuxin; Nishihara, Arisa; Haruta, Shin Microbes and Environments, Vol. 36, Issue 2 https://doi.org/10.1264/jsme2.ME21018	journal	January 2021
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Extremely thermophilic microorganisms as metabolic engineering platforms for production of fuels and industrial chemicals Zeldes, Benjamin M.; Keller, Matthew W.; Loder, Andrew J. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01209	journal	November 2015
“Freezing” Thermophiles: From One Temperature Extreme to Another Milojevic, Tetyana; Cramm, Margaret Anne; Hubert, Casey R. J. Microorganisms, Vol. 10, Issue 12 https://doi.org/10.3390/microorganisms10122417	journal	December 2022
Insights into Thermophilic Plant Biomass Hydrolysis from Caldicellulosiruptor Systems Biology Blumer-Schuette, Sara E. Microorganisms, Vol. 8, Issue 3 https://doi.org/10.3390/microorganisms8030385	journal	March 2020

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59 BASIC BIOLOGICAL SCIENCES
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Microbiology
Thermoanaerobacterales
bacteria
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fermentative anaerobes
phylogeny
thermophiles

Whither the genus Caldicellulosiruptor and the order Thermoanaerobacterales: phylogeny, taxonomy, ecology, and phenotype

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