The <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence

ABSTRACT Quorum sensing is a chemical communication process in which bacteria use the production, release, and detection of signal molecules called autoinducers to orchestrate collective behaviors. The human pathogen Vibrio cholerae requires quorum sensing to infect the small intestine. There, V. ch...

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Autores principales: Ameya A. Mashruwala, Bonnie L. Bassler
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:4e8d6e28526a4e45a76956e4c1a756f02021-11-15T15:56:43ZThe <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence10.1128/mBio.01572-202150-7511https://doaj.org/article/4e8d6e28526a4e45a76956e4c1a756f02020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01572-20https://doaj.org/toc/2150-7511ABSTRACT Quorum sensing is a chemical communication process in which bacteria use the production, release, and detection of signal molecules called autoinducers to orchestrate collective behaviors. The human pathogen Vibrio cholerae requires quorum sensing to infect the small intestine. There, V. cholerae encounters the absence of oxygen and the presence of bile salts. We show that these two stimuli differentially affect quorum-sensing function and, in turn, V. cholerae pathogenicity. First, during anaerobic growth, V. cholerae does not produce the CAI-1 autoinducer, while it continues to produce the DPO autoinducer, suggesting that CAI-1 may encode information specific to the aerobic lifestyle of V. cholerae. Second, the quorum-sensing receptor-transcription factor called VqmA, which detects the DPO autoinducer, also detects the lack of oxygen and the presence of bile salts. Detection occurs via oxygen-, bile salt-, and redox-responsive disulfide bonds that alter VqmA DNA binding activity. We propose that VqmA serves as an information processing hub that integrates quorum-sensing information, redox status, the presence or absence of oxygen, and host cues. In response to the information acquired through this mechanism, V. cholerae appropriately modulates its virulence output. IMPORTANCE Quorum sensing (QS) is a process of chemical communication that bacteria use to orchestrate collective behaviors. QS communication relies on chemical signal molecules called autoinducers. QS regulates virulence in Vibrio cholerae, the causative agent of the disease cholera. Transit into the human small intestine, the site of cholera infection, exposes V. cholerae to the host environment. In this study, we show that the combination of two stimuli encountered in the small intestine, the absence of oxygen and the presence of host-produced bile salts, impinge on V. cholerae QS function and, in turn, pathogenicity. We suggest that possessing a QS system that is responsive to multiple environmental, host, and cell density cues enables V. cholerae to fine-tune its virulence capacity in the human intestine.Ameya A. MashruwalaBonnie L. BasslerAmerican Society for MicrobiologyarticleVibrio choleraeVqmAoxygenpathogenesisquorum sensingredoxMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution DOAJ
collection DOAJ
language EN
topic Vibrio cholerae
VqmA
oxygen
pathogenesis
quorum sensing
redox
Microbiology
QR1-502
spellingShingle Vibrio cholerae
VqmA
oxygen
pathogenesis
quorum sensing
redox
Microbiology
QR1-502
Ameya A. Mashruwala
Bonnie L. Bassler
The <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence
description ABSTRACT Quorum sensing is a chemical communication process in which bacteria use the production, release, and detection of signal molecules called autoinducers to orchestrate collective behaviors. The human pathogen Vibrio cholerae requires quorum sensing to infect the small intestine. There, V. cholerae encounters the absence of oxygen and the presence of bile salts. We show that these two stimuli differentially affect quorum-sensing function and, in turn, V. cholerae pathogenicity. First, during anaerobic growth, V. cholerae does not produce the CAI-1 autoinducer, while it continues to produce the DPO autoinducer, suggesting that CAI-1 may encode information specific to the aerobic lifestyle of V. cholerae. Second, the quorum-sensing receptor-transcription factor called VqmA, which detects the DPO autoinducer, also detects the lack of oxygen and the presence of bile salts. Detection occurs via oxygen-, bile salt-, and redox-responsive disulfide bonds that alter VqmA DNA binding activity. We propose that VqmA serves as an information processing hub that integrates quorum-sensing information, redox status, the presence or absence of oxygen, and host cues. In response to the information acquired through this mechanism, V. cholerae appropriately modulates its virulence output. IMPORTANCE Quorum sensing (QS) is a process of chemical communication that bacteria use to orchestrate collective behaviors. QS communication relies on chemical signal molecules called autoinducers. QS regulates virulence in Vibrio cholerae, the causative agent of the disease cholera. Transit into the human small intestine, the site of cholera infection, exposes V. cholerae to the host environment. In this study, we show that the combination of two stimuli encountered in the small intestine, the absence of oxygen and the presence of host-produced bile salts, impinge on V. cholerae QS function and, in turn, pathogenicity. We suggest that possessing a QS system that is responsive to multiple environmental, host, and cell density cues enables V. cholerae to fine-tune its virulence capacity in the human intestine.
format article
author Ameya A. Mashruwala
Bonnie L. Bassler
author_facet Ameya A. Mashruwala
Bonnie L. Bassler
author_sort Ameya A. Mashruwala
title The <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence
title_short The <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence
title_full The <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence
title_fullStr The <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence
title_full_unstemmed The <named-content content-type="genus-species">Vibrio cholerae</named-content> Quorum-Sensing Protein VqmA Integrates Cell Density, Environmental, and Host-Derived Cues into the Control of Virulence
title_sort <named-content content-type="genus-species">vibrio cholerae</named-content> quorum-sensing protein vqma integrates cell density, environmental, and host-derived cues into the control of virulence
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/4e8d6e28526a4e45a76956e4c1a756f0
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