The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing

A common strategy by which bacterial pathogens reside in humans is by shifting from a virulent lifestyle, (systemic infection), to a dormant carrier state. Two major serovars of Salmonella enterica, Typhi and Typhimurium, have evolved a two-component regulatory system to exist inside Salmonella-cont...

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Main Authors: Stuti K Desai, Ricksen S Winardhi, Saravanan Periasamy, Michal M Dykas, Yan Jie, Linda J Kenney
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/10747
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spelling doaj-b4e9c530c2dd4fa785f383d6c581130d2021-05-05T00:14:53ZengeLife Sciences Publications LtdeLife2050-084X2016-02-01510.7554/eLife.10747The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencingStuti K Desai0Ricksen S Winardhi1Saravanan Periasamy2Michal M Dykas3https://orcid.org/0000-0001-5933-314XYan Jie4Linda J Kenney5Mechanobiology Institute, National University of Singapore, Singapore, SingaporeMechanobiology Institute, National University of Singapore, Singapore, Singapore; Department of Physics, National University of Singapore, Singapore, SingaporeSingapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University, Singapore, SingaporeNanoscience and Nanotechnology Institute, National University of Singapore, Singapore, Singapore; Graduate School for Integrative Sciences and Engineering, National University of Singapore, Singapore, SingaporeMechanobiology Institute, National University of Singapore, Singapore, Singapore; Department of Physics, National University of Singapore, Singapore, SingaporeMechanobiology Institute, National University of Singapore, Singapore, Singapore; Jesse Brown Veterans Affairs Medical Center, University of Illinois-Chicago, Chicago, United States; Department of Microbiology and Immunology, University of Illinois-Chicago, Chicago, United StatesA common strategy by which bacterial pathogens reside in humans is by shifting from a virulent lifestyle, (systemic infection), to a dormant carrier state. Two major serovars of Salmonella enterica, Typhi and Typhimurium, have evolved a two-component regulatory system to exist inside Salmonella-containing vacuoles in the macrophage, as well as to persist as asymptomatic biofilms in the gallbladder. Here we present evidence that SsrB, a transcriptional regulator encoded on the SPI-2 pathogenicity-island, determines the switch between these two lifestyles by controlling ancestral and horizontally-acquired genes. In the acidic macrophage vacuole, the kinase SsrA phosphorylates SsrB, and SsrB~P relieves silencing of virulence genes and activates their transcription. In the absence of SsrA, unphosphorylated SsrB directs transcription of factors required for biofilm formation specifically by activating csgD (agfD), the master biofilm regulator by disrupting the silenced, H-NS-bound promoter. Anti-silencing mechanisms thus control the switch between opposing lifestyles.https://elifesciences.org/articles/10747biofilmsalmonella typhimuriumtwo-component regulatory systemssrA/BcsgD/agfDH-NS
collection DOAJ
language English
format Article
sources DOAJ
author Stuti K Desai
Ricksen S Winardhi
Saravanan Periasamy
Michal M Dykas
Yan Jie
Linda J Kenney
spellingShingle Stuti K Desai
Ricksen S Winardhi
Saravanan Periasamy
Michal M Dykas
Yan Jie
Linda J Kenney
The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing
eLife
biofilm
salmonella typhimurium
two-component regulatory system
ssrA/B
csgD/agfD
H-NS
author_facet Stuti K Desai
Ricksen S Winardhi
Saravanan Periasamy
Michal M Dykas
Yan Jie
Linda J Kenney
author_sort Stuti K Desai
title The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing
title_short The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing
title_full The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing
title_fullStr The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing
title_full_unstemmed The horizontally-acquired response regulator SsrB drives a Salmonella lifestyle switch by relieving biofilm silencing
title_sort horizontally-acquired response regulator ssrb drives a salmonella lifestyle switch by relieving biofilm silencing
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2016-02-01
description A common strategy by which bacterial pathogens reside in humans is by shifting from a virulent lifestyle, (systemic infection), to a dormant carrier state. Two major serovars of Salmonella enterica, Typhi and Typhimurium, have evolved a two-component regulatory system to exist inside Salmonella-containing vacuoles in the macrophage, as well as to persist as asymptomatic biofilms in the gallbladder. Here we present evidence that SsrB, a transcriptional regulator encoded on the SPI-2 pathogenicity-island, determines the switch between these two lifestyles by controlling ancestral and horizontally-acquired genes. In the acidic macrophage vacuole, the kinase SsrA phosphorylates SsrB, and SsrB~P relieves silencing of virulence genes and activates their transcription. In the absence of SsrA, unphosphorylated SsrB directs transcription of factors required for biofilm formation specifically by activating csgD (agfD), the master biofilm regulator by disrupting the silenced, H-NS-bound promoter. Anti-silencing mechanisms thus control the switch between opposing lifestyles.
topic biofilm
salmonella typhimurium
two-component regulatory system
ssrA/B
csgD/agfD
H-NS
url https://elifesciences.org/articles/10747
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