Acetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation

ABSTRACT Volatiles are small air-transmittable chemicals with diverse biological activities. In this study, we showed that volatiles produced by the bacterium Bacillus subtilis had a profound effect on biofilm formation of neighboring B. subtilis cells that grew in proximity but were physically sepa...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Yun Chen, Kevin Gozzi, Fang Yan, Yunrong Chai
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2015
Materias:
Acceso en línea:https://doaj.org/article/726e5a1ddc03496cadcef2794c162e84
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:726e5a1ddc03496cadcef2794c162e84
record_format dspace
spelling oai:doaj.org-article:726e5a1ddc03496cadcef2794c162e842021-11-15T15:49:03ZAcetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation10.1128/mBio.00392-152150-7511https://doaj.org/article/726e5a1ddc03496cadcef2794c162e842015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00392-15https://doaj.org/toc/2150-7511ABSTRACT Volatiles are small air-transmittable chemicals with diverse biological activities. In this study, we showed that volatiles produced by the bacterium Bacillus subtilis had a profound effect on biofilm formation of neighboring B. subtilis cells that grew in proximity but were physically separated. We further demonstrated that one such volatile, acetic acid, is particularly potent in stimulating biofilm formation. Multiple lines of genetic evidence based on B. subtilis mutants that are defective in either acetic acid production or transportation suggest that B. subtilis uses acetic acid as a metabolic signal to coordinate the timing of biofilm formation. Lastly, we investigated how B. subtilis cells sense and respond to acetic acid in regulating biofilm formation. We showed the possible involvement of three sets of genes (ywbHG, ysbAB, and yxaKC), all encoding putative holin-antiholin-like proteins, in cells responding to acetic acid and stimulating biofilm formation. All three sets of genes were induced by acetate. A mutant with a triple mutation of those genes showed a severe delay in biofilm formation, whereas a strain overexpressing ywbHG showed early and robust biofilm formation. Results of our studies suggest that B. subtilis and possibly other bacteria use acetic acid as a metabolic signal to regulate biofilm formation as well as a quorum-sensing-like airborne signal to coordinate the timing of biofilm formation by physically separated cells in the community. IMPORTANCE Volatiles are small, air-transmittable molecules produced by all kingdoms of organisms including bacteria. Volatiles possess diverse biological activities and play important roles in bacteria-bacteria and bacteria-host interactions. Although volatiles can be used as a novel and important way of cell-cell communication due to their air-transmittable nature, little is known about how the volatile-mediated signaling mechanism works. In this study, we demonstrate that the bacterium Bacillus subtilis uses one such volatile, acetic acid, as a quorum-sensing-like signal to coordinate the timing of the formation of structurally complex cell communities, also known as biofilms. We further characterized the molecular mechanisms of how B. subtilis responds to acetic acid in stimulating biofilm formation. Our study also suggests that acetic acid may be used as a volatile signal for cross-species communication.Yun ChenKevin GozziFang YanYunrong ChaiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Yun Chen
Kevin Gozzi
Fang Yan
Yunrong Chai
Acetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation
description ABSTRACT Volatiles are small air-transmittable chemicals with diverse biological activities. In this study, we showed that volatiles produced by the bacterium Bacillus subtilis had a profound effect on biofilm formation of neighboring B. subtilis cells that grew in proximity but were physically separated. We further demonstrated that one such volatile, acetic acid, is particularly potent in stimulating biofilm formation. Multiple lines of genetic evidence based on B. subtilis mutants that are defective in either acetic acid production or transportation suggest that B. subtilis uses acetic acid as a metabolic signal to coordinate the timing of biofilm formation. Lastly, we investigated how B. subtilis cells sense and respond to acetic acid in regulating biofilm formation. We showed the possible involvement of three sets of genes (ywbHG, ysbAB, and yxaKC), all encoding putative holin-antiholin-like proteins, in cells responding to acetic acid and stimulating biofilm formation. All three sets of genes were induced by acetate. A mutant with a triple mutation of those genes showed a severe delay in biofilm formation, whereas a strain overexpressing ywbHG showed early and robust biofilm formation. Results of our studies suggest that B. subtilis and possibly other bacteria use acetic acid as a metabolic signal to regulate biofilm formation as well as a quorum-sensing-like airborne signal to coordinate the timing of biofilm formation by physically separated cells in the community. IMPORTANCE Volatiles are small, air-transmittable molecules produced by all kingdoms of organisms including bacteria. Volatiles possess diverse biological activities and play important roles in bacteria-bacteria and bacteria-host interactions. Although volatiles can be used as a novel and important way of cell-cell communication due to their air-transmittable nature, little is known about how the volatile-mediated signaling mechanism works. In this study, we demonstrate that the bacterium Bacillus subtilis uses one such volatile, acetic acid, as a quorum-sensing-like signal to coordinate the timing of the formation of structurally complex cell communities, also known as biofilms. We further characterized the molecular mechanisms of how B. subtilis responds to acetic acid in stimulating biofilm formation. Our study also suggests that acetic acid may be used as a volatile signal for cross-species communication.
format article
author Yun Chen
Kevin Gozzi
Fang Yan
Yunrong Chai
author_facet Yun Chen
Kevin Gozzi
Fang Yan
Yunrong Chai
author_sort Yun Chen
title Acetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation
title_short Acetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation
title_full Acetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation
title_fullStr Acetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation
title_full_unstemmed Acetic Acid Acts as a Volatile Signal To Stimulate Bacterial Biofilm Formation
title_sort acetic acid acts as a volatile signal to stimulate bacterial biofilm formation
publisher American Society for Microbiology
publishDate 2015
url https://doaj.org/article/726e5a1ddc03496cadcef2794c162e84
work_keys_str_mv AT yunchen aceticacidactsasavolatilesignaltostimulatebacterialbiofilmformation
AT kevingozzi aceticacidactsasavolatilesignaltostimulatebacterialbiofilmformation
AT fangyan aceticacidactsasavolatilesignaltostimulatebacterialbiofilmformation
AT yunrongchai aceticacidactsasavolatilesignaltostimulatebacterialbiofilmformation
_version_ 1718427464860958720