Role of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species

ABSTRACT Capsular polysaccharide (CPS) is essential for the dispersal of biofilms formed by the pathogenic bacterium Vibrio vulnificus. CPS production is induced by the quorum-sensing (QS) master regulator SmcR when biofilms mature. However, V. vulnificus biofilms formed under heat shock conditions...

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Autores principales: Kyung-Jo Lee, You-Chul Jung, Soon-Jung Park, Kyu-Ho Lee
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:d4fd1872f57746efa24c2402018543322021-11-15T15:53:26ZRole of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species10.1128/mBio.02086-172150-7511https://doaj.org/article/d4fd1872f57746efa24c2402018543322018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02086-17https://doaj.org/toc/2150-7511ABSTRACT Capsular polysaccharide (CPS) is essential for the dispersal of biofilms formed by the pathogenic bacterium Vibrio vulnificus. CPS production is induced by the quorum-sensing (QS) master regulator SmcR when biofilms mature. However, V. vulnificus biofilms formed under heat shock conditions did not exhibit the dispersion stage. Transcripts of the CPS gene cluster were at basal levels in the heat-exposed cell owing to reduced cellular levels of SmcR. At least two proteases induced by heat shock, ClpPA and Lon, were responsible for determining the instability of SmcR. In vitro and in vivo assays demonstrated that SmcR levels were regulated via proteolysis by these proteases, with preferential proteolysis of monomeric SmcR. Thus, CPS production was not induced by QS when bacteria were heat treated. Further studies performed with other Vibrio species demonstrated that high temperature deactivated the QS circuits by increased proteolysis of their QS master regulators, thus resulting in alterations to the QS-regulated phenotypes, including biofilm formation. IMPORTANCE The term "quorum-sensing mechanism" is used to describe diverse bacterial cell density-dependent activities that are achieved by sensing of the signaling molecules and subsequent signal transduction to the master regulators. These well-known bacterial regulatory systems regulate the expression of diverse virulence factors and the construction of biofilms in pathogenic bacteria. There have been numerous studies designed to control bacterial quorum sensing by using small molecules to antagonize the quorum-sensing regulatory components or to interfere with the signaling molecules. In the present study, we showed that the quorum-sensing regulatory circuits of pathogenic Vibrio species were deactivated by heat shock treatment via highly increased proteolysis of the master transcription factors. Our results showed a new mode of quorum deactivation which can be achieved under conditions of high but nonlethal temperature even if the ambient signaling molecules may reach the levels representing high cell density.Kyung-Jo LeeYou-Chul JungSoon-Jung ParkKyu-Ho LeeAmerican Society for MicrobiologyarticleClpPALonquorum-sensing master regulatorsVibrio speciesMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution DOAJ
collection DOAJ
language EN
topic ClpPA
Lon
quorum-sensing master regulators
Vibrio species
Microbiology
QR1-502
spellingShingle ClpPA
Lon
quorum-sensing master regulators
Vibrio species
Microbiology
QR1-502
Kyung-Jo Lee
You-Chul Jung
Soon-Jung Park
Kyu-Ho Lee
Role of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species
description ABSTRACT Capsular polysaccharide (CPS) is essential for the dispersal of biofilms formed by the pathogenic bacterium Vibrio vulnificus. CPS production is induced by the quorum-sensing (QS) master regulator SmcR when biofilms mature. However, V. vulnificus biofilms formed under heat shock conditions did not exhibit the dispersion stage. Transcripts of the CPS gene cluster were at basal levels in the heat-exposed cell owing to reduced cellular levels of SmcR. At least two proteases induced by heat shock, ClpPA and Lon, were responsible for determining the instability of SmcR. In vitro and in vivo assays demonstrated that SmcR levels were regulated via proteolysis by these proteases, with preferential proteolysis of monomeric SmcR. Thus, CPS production was not induced by QS when bacteria were heat treated. Further studies performed with other Vibrio species demonstrated that high temperature deactivated the QS circuits by increased proteolysis of their QS master regulators, thus resulting in alterations to the QS-regulated phenotypes, including biofilm formation. IMPORTANCE The term "quorum-sensing mechanism" is used to describe diverse bacterial cell density-dependent activities that are achieved by sensing of the signaling molecules and subsequent signal transduction to the master regulators. These well-known bacterial regulatory systems regulate the expression of diverse virulence factors and the construction of biofilms in pathogenic bacteria. There have been numerous studies designed to control bacterial quorum sensing by using small molecules to antagonize the quorum-sensing regulatory components or to interfere with the signaling molecules. In the present study, we showed that the quorum-sensing regulatory circuits of pathogenic Vibrio species were deactivated by heat shock treatment via highly increased proteolysis of the master transcription factors. Our results showed a new mode of quorum deactivation which can be achieved under conditions of high but nonlethal temperature even if the ambient signaling molecules may reach the levels representing high cell density.
format article
author Kyung-Jo Lee
You-Chul Jung
Soon-Jung Park
Kyu-Ho Lee
author_facet Kyung-Jo Lee
You-Chul Jung
Soon-Jung Park
Kyu-Ho Lee
author_sort Kyung-Jo Lee
title Role of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species
title_short Role of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species
title_full Role of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species
title_fullStr Role of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species
title_full_unstemmed Role of Heat Shock Proteases in Quorum-Sensing-Mediated Regulation of Biofilm Formation by <italic toggle="yes">Vibrio</italic> Species
title_sort role of heat shock proteases in quorum-sensing-mediated regulation of biofilm formation by <italic toggle="yes">vibrio</italic> species
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/d4fd1872f57746efa24c240201854332
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