Thermophilic Dehalococcoidia with unusual traits shed light on an unexpected past

Palmer, Marike; Covington, Jonathan K.; Zhou, En-Min; Thomas, Scott C.; Habib, Neeli; Seymour, Cale O.; Lai, Dengxun; Johnston, Juliet; Hashimi, Ameena; Jiao, Jian-Yu; Muok, Alise R.; Liu, Lan; Xian, Wen-Dong; Zhi, Xiao-Yang; Li, Meng-Meng; Silva, Leslie P.; Bowen, Benjamin P.; Louie, Katherine; Briegel, Ariane; Pett-Ridge, Jennifer; Weber, Peter K.; Tocheva, Elitza I.; Woyke, Tanja; Northen, Trent R.; Mayali, Xavier; Li, Wen-Jun; Hedlund, Brian P.

doi:10.1038/s41396-023-01405-0

Title: Thermophilic Dehalococcoidia with unusual traits shed light on an unexpected past

Journal Article · 10 April 2023 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-023-01405-0 · OSTI ID:1969437

;

; Habib, Neeli; Seymour, Cale O.;

; Johnston, Juliet; Hashimi, Ameena;

; Muok, Alise R.;

; Xian, Wen-Dong;

; Li, Meng-Meng; Silva, Leslie P.;

; Louie, Katherine;

;

Abstract Although the phylum Chloroflexota is ubiquitous, its biology and evolution are poorly understood due to limited cultivability. Here, we isolated two motile, thermophilic bacteria from hot spring sediments belonging to the genus Tepidiforma and class Dehalococcoidia within the phylum Chloroflexota. A combination of cryo-electron tomography, exometabolomics, and cultivation experiments using stable isotopes of carbon revealed three unusual traits: flagellar motility, a peptidoglycan-containing cell envelope, and heterotrophic activity on aromatics and plant-associated compounds. Outside of this genus, flagellar motility has not been observed in Chloroflexota, and peptidoglycan-containing cell envelopes have not been described in Dehalococcoidia. Although these traits are unusual among cultivated Chloroflexota and Dehalococcoidia, ancestral character state reconstructions showed flagellar motility and peptidoglycan-containing cell envelopes were ancestral within the Dehalococcoidia, and subsequently lost prior to a major adaptive radiation of Dehalococcoidia into marine environments. However, despite the predominantly vertical evolutionary histories of flagellar motility and peptidoglycan biosynthesis, the evolution of enzymes for degradation of aromatics and plant-associated compounds was predominantly horizontal and complex. Together, the presence of these unusual traits in Dehalococcoidia and their evolutionary histories raise new questions about the timing and selective forces driving their successful niche expansion into global oceans.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: National Aeronautics and Space Administration (NASA); National Natural Science Foundation of China (NSFC); National Science Foundation (NSF); Natural Sciences and Engineering Research Council of Canada (NSERC); USDOE; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC02-05CH11231; AC52-07NA27344

OSTI ID:: 1969437

Report Number(s):: LLNL--JRNL-841058

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 7 Vol. 17; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Bacteria
Metabolomics
Microbial ecology
Phylogenetics
Sequencing

Title: Thermophilic Dehalococcoidia with unusual traits shed light on an unexpected past

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