Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria

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 p...

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Autores principales:	Jennifer Hiras, Sunil V. Sharma, Vidhyavathi Raman, Ryan A. J. Tinson, Miriam Arbach, Dominic F. Rodrigues, Javiera Norambuena, Chris J. Hamilton, Thomas E. Hanson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	cellular redox status Chlorobaculum tepidum chlorobiaceae low molecular weight thiol sulfur Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d36b29d461834c37bfe7f6803e0f1170
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spelling	oai:doaj.org-article:d36b29d461834c37bfe7f6803e0f11702021-11-15T15:52:19ZPhysiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria10.1128/mBio.01603-182150-7511https://doaj.org/article/d36b29d461834c37bfe7f6803e0f11702018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01603-18https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Low-molecular-weight thiols are key metabolites that participate in many basic cellular processes: central metabolism, detoxification, and oxidative stress resistance. Here we describe a new thiol, N-methyl-bacillithiol, found in an anaerobic phototrophic bacterium and identify a gene that is responsible for its synthesis from bacillithiol, the main thiol metabolite in many Gram-positive bacteria. We show that the presence or absence of this gene in a sequenced genome accurately predicts thiol content in distantly related bacteria. On the basis of these results, we analyzed genome data and predict that bacillithiol and its derivatives are the most widely distributed thiol metabolites in biology.Jennifer HirasSunil V. SharmaVidhyavathi RamanRyan A. J. TinsonMiriam ArbachDominic F. RodriguesJaviera NorambuenaChris J. HamiltonThomas E. HansonAmerican Society for Microbiologyarticlecellular redox statusChlorobaculum tepidumchlorobiaceaelow molecular weight thiolsulfurMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	cellular redox status Chlorobaculum tepidum chlorobiaceae low molecular weight thiol sulfur Microbiology QR1-502
spellingShingle	cellular redox status Chlorobaculum tepidum chlorobiaceae low molecular weight thiol sulfur Microbiology QR1-502 Jennifer Hiras Sunil V. Sharma Vidhyavathi Raman Ryan A. J. Tinson Miriam Arbach Dominic F. Rodrigues Javiera Norambuena Chris J. Hamilton Thomas E. Hanson Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria
description	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. IMPORTANCE Low-molecular-weight thiols are key metabolites that participate in many basic cellular processes: central metabolism, detoxification, and oxidative stress resistance. Here we describe a new thiol, N-methyl-bacillithiol, found in an anaerobic phototrophic bacterium and identify a gene that is responsible for its synthesis from bacillithiol, the main thiol metabolite in many Gram-positive bacteria. We show that the presence or absence of this gene in a sequenced genome accurately predicts thiol content in distantly related bacteria. On the basis of these results, we analyzed genome data and predict that bacillithiol and its derivatives are the most widely distributed thiol metabolites in biology.
format	article
author	Jennifer Hiras Sunil V. Sharma Vidhyavathi Raman Ryan A. J. Tinson Miriam Arbach Dominic F. Rodrigues Javiera Norambuena Chris J. Hamilton Thomas E. Hanson
author_facet	Jennifer Hiras Sunil V. Sharma Vidhyavathi Raman Ryan A. J. Tinson Miriam Arbach Dominic F. Rodrigues Javiera Norambuena Chris J. Hamilton Thomas E. Hanson
author_sort	Jennifer Hiras
title	Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria
title_short	Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria
title_full	Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria
title_fullStr	Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria
title_full_unstemmed	Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria
title_sort	physiological studies of <italic toggle="yes">chlorobiaceae</italic> suggest that bacillithiol derivatives are the most widespread thiols in bacteria
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d36b29d461834c37bfe7f6803e0f1170
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Physiological Studies of <italic toggle="yes">Chlorobiaceae</italic> Suggest that Bacillithiol Derivatives Are the Most Widespread Thiols in Bacteria

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