A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics

ABSTRACT Antibiotics produced by bacteria play important roles in microbial interactions and competition Antibiosis can induce resistance mechanisms in target organisms, and at sublethal doses, antibiotics have been shown to globally alter gene expression patterns. Here, we show that hygromycin A fr...

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Autores principales:	Gabriel L. Lozano, Changhui Guan, Yanzhuan Cao, Bradley R. Borlee, Nichole A. Broderick, Eric V. Stabb, Jo Handelsman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	sublethal concentration antibiotics two-component regulatory system Streptomyces microbe-microbe interactions translation inhibition Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/18ee74f479c549009ac47c2ea8a76be4
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spelling	oai:doaj.org-article:18ee74f479c549009ac47c2ea8a76be42021-11-15T15:56:46ZA Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics10.1128/mBio.00948-202150-7511https://doaj.org/article/18ee74f479c549009ac47c2ea8a76be42020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00948-20https://doaj.org/toc/2150-7511ABSTRACT Antibiotics produced by bacteria play important roles in microbial interactions and competition Antibiosis can induce resistance mechanisms in target organisms, and at sublethal doses, antibiotics have been shown to globally alter gene expression patterns. Here, we show that hygromycin A from Streptomyces sp. strain 2AW. induces Chromobacterium violaceum ATCC 31532 to produce the purple antibiotic violacein. Sublethal doses of other antibiotics that similarly target the polypeptide elongation step of translation likewise induced violacein production, unlike antibiotics with different targets. C. violaceum biofilm formation and virulence against Drosophila melanogaster were also induced by translation-inhibiting antibiotics, and we identified an antibiotic-induced response (air) two-component regulatory system that is required for these responses. Genetic analyses indicated a connection between the Air system, quorum-dependent signaling, and the negative regulator VioS, leading us to propose a model for induction of violacein production. This work suggests a novel mechanism of interspecies interaction in which a bacterium produces an antibiotic in response to inhibition by another bacterium and supports the role of antibiotics as signal molecules. IMPORTANCE Secondary metabolites play important roles in microbial communities, but their natural functions are often unknown and may be more complex than appreciated. While compounds with antibiotic activity are often assumed to underlie microbial competition, they may alternatively act as signal molecules. In either scenario, microorganisms might evolve responses to sublethal concentrations of these metabolites, either to protect themselves from inhibition or to change certain behaviors in response to the local abundance of another species. Here, we report that violacein production by C. violaceum ATCC 31532 is induced in response to hygromycin A from Streptomyces sp. 2AW, and we show that this response is dependent on inhibition of translational polypeptide elongation and a previously uncharacterized two-component regulatory system. The breadth of the transcriptional response beyond violacein induction suggests a surprisingly complex metabolite-mediated microbe-microbe interaction and supports the hypothesis that antibiotics evolved as signal molecules. These novel insights will inform predictive models of soil community dynamics and the unintended effects of clinical antibiotic administration.Gabriel L. LozanoChanghui GuanYanzhuan CaoBradley R. BorleeNichole A. BroderickEric V. StabbJo HandelsmanAmerican Society for Microbiologyarticlesublethal concentration antibioticstwo-component regulatory systemStreptomycesmicrobe-microbe interactionstranslation inhibitionMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	sublethal concentration antibiotics two-component regulatory system Streptomyces microbe-microbe interactions translation inhibition Microbiology QR1-502
spellingShingle	sublethal concentration antibiotics two-component regulatory system Streptomyces microbe-microbe interactions translation inhibition Microbiology QR1-502 Gabriel L. Lozano Changhui Guan Yanzhuan Cao Bradley R. Borlee Nichole A. Broderick Eric V. Stabb Jo Handelsman A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics
description	ABSTRACT Antibiotics produced by bacteria play important roles in microbial interactions and competition Antibiosis can induce resistance mechanisms in target organisms, and at sublethal doses, antibiotics have been shown to globally alter gene expression patterns. Here, we show that hygromycin A from Streptomyces sp. strain 2AW. induces Chromobacterium violaceum ATCC 31532 to produce the purple antibiotic violacein. Sublethal doses of other antibiotics that similarly target the polypeptide elongation step of translation likewise induced violacein production, unlike antibiotics with different targets. C. violaceum biofilm formation and virulence against Drosophila melanogaster were also induced by translation-inhibiting antibiotics, and we identified an antibiotic-induced response (air) two-component regulatory system that is required for these responses. Genetic analyses indicated a connection between the Air system, quorum-dependent signaling, and the negative regulator VioS, leading us to propose a model for induction of violacein production. This work suggests a novel mechanism of interspecies interaction in which a bacterium produces an antibiotic in response to inhibition by another bacterium and supports the role of antibiotics as signal molecules. IMPORTANCE Secondary metabolites play important roles in microbial communities, but their natural functions are often unknown and may be more complex than appreciated. While compounds with antibiotic activity are often assumed to underlie microbial competition, they may alternatively act as signal molecules. In either scenario, microorganisms might evolve responses to sublethal concentrations of these metabolites, either to protect themselves from inhibition or to change certain behaviors in response to the local abundance of another species. Here, we report that violacein production by C. violaceum ATCC 31532 is induced in response to hygromycin A from Streptomyces sp. 2AW, and we show that this response is dependent on inhibition of translational polypeptide elongation and a previously uncharacterized two-component regulatory system. The breadth of the transcriptional response beyond violacein induction suggests a surprisingly complex metabolite-mediated microbe-microbe interaction and supports the hypothesis that antibiotics evolved as signal molecules. These novel insights will inform predictive models of soil community dynamics and the unintended effects of clinical antibiotic administration.
format	article
author	Gabriel L. Lozano Changhui Guan Yanzhuan Cao Bradley R. Borlee Nichole A. Broderick Eric V. Stabb Jo Handelsman
author_facet	Gabriel L. Lozano Changhui Guan Yanzhuan Cao Bradley R. Borlee Nichole A. Broderick Eric V. Stabb Jo Handelsman
author_sort	Gabriel L. Lozano
title	A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics
title_short	A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics
title_full	A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics
title_fullStr	A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics
title_full_unstemmed	A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics
title_sort	chemical counterpunch: <named-content content-type="genus-species">chromobacterium violaceum</named-content> atcc 31532 produces violacein in response to translation-inhibiting antibiotics
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/18ee74f479c549009ac47c2ea8a76be4
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A Chemical Counterpunch: <named-content content-type="genus-species">Chromobacterium violaceum</named-content> ATCC 31532 Produces Violacein in Response to Translation-Inhibiting Antibiotics

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