Physiological studies of Chlorobiaceae suggest that bacillithiol derivatives are the most widespread thiols in bacteria

Jennifer Hiras, Sunil V. Sharma, Vidhyavathi Raman, Ryan A. J. Tinson, Miriam Arbach, Dominic F. Rodrigues, Javiera Norambuena, Chris J. Hamilton, Thomas E. Hanson

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    Abstract

    Low-molecular-weight (LMW) thiols mediate redox homeostasis and the detoxification of chemical stressors. Despite their essential functions, the distribution of LMW thiols across cellular life has not yet been defined. LMW thiols are also thought to play a central role in sulfur oxidation pathways in phototrophic bacteria, including the Chlorobiaceae. Here we show that Chlorobaculum tepidum synthesizes a novel LMW thiol with a mass of 412 ± 1 Da corresponding to a molecular formula of C14H24N2O10S, which suggests that the new LMW thiol is closely related to bacillithiol (BSH), the major LMW thiol of low-G+C Gram-positive bacteria. The Cba. tepidum LMW thiol structure was N-methyl-bacillithiol (N-Me-BSH), methylated on the cysteine nitrogen, the fourth instance of this modification in metabolism. Orthologs of bacillithiol biosynthetic genes in the Cba. tepidum genome and the CT1040 gene product, N-Me-BSH synthase, were required for N-Me-BSH synthesis. N-Me-BSH was found in all Chlorobiaceae examined as well as Polaribacter sp. strain MED152, a member of the Bacteroidetes. A comparative genomic analysis indicated that BSH/N-Me-BSH is synthesized not only by members of the Chlorobiaceae, Bacteroidetes, Deinococcus-Thermus, and Firmicutes but also by Acidobacteria, Chlamydiae, Gemmatimonadetes, and Proteobacteria. Thus, BSH and derivatives appear to be the most broadly distributed LMW thiols in biology.
    Original languageEnglish
    Article numbere01603-18
    JournalmBIO
    Volume9
    Issue number6
    DOIs
    Publication statusPublished - 27 Nov 2018

    Keywords

    • cellular redox status
    • Chlorobaculum tepidum
    • chlorobiaceae
    • low molecular weight thiol
    • sulfur

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