Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.

Edwardsiella piscicida is a leading fish pathogen that causes significant economic loses in the aquaculture industry. The pathogen depends on type III and type VI secretion systems (T3/T6SS) for growth and virulence in fish and the expression of both systems is controlled by the EsrB transcription a...

Full description

Bibliographic Details
Main Authors: Kaiyu Yin, Yunpeng Guan, Ruiqing Ma, Lifan Wei, Bing Liu, Xiaohong Liu, Xiangshan Zhou, Yue Ma, Yuanxing Zhang, Matthew K Waldor, Qiyao Wang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-08-01
Series:PLoS Pathogens
Online Access:http://europepmc.org/articles/PMC6136808?pdf=render
_version_ 1830287469897056256
author Kaiyu Yin
Yunpeng Guan
Ruiqing Ma
Lifan Wei
Bing Liu
Xiaohong Liu
Xiangshan Zhou
Yue Ma
Yuanxing Zhang
Matthew K Waldor
Qiyao Wang
author_facet Kaiyu Yin
Yunpeng Guan
Ruiqing Ma
Lifan Wei
Bing Liu
Xiaohong Liu
Xiangshan Zhou
Yue Ma
Yuanxing Zhang
Matthew K Waldor
Qiyao Wang
author_sort Kaiyu Yin
collection DOAJ
description Edwardsiella piscicida is a leading fish pathogen that causes significant economic loses in the aquaculture industry. The pathogen depends on type III and type VI secretion systems (T3/T6SS) for growth and virulence in fish and the expression of both systems is controlled by the EsrB transcription activator. Here, we performed a Tn-seq-based screen to uncover factors that govern esrB expression. Unexpectedly, we discovered that RpoS antagonizes esrB expression and thereby inhibits production of E. piscicida's T3/T6SS. Using in vitro transcription assays, we showed that RpoS can block RpoD-mediated transcription of esrB. ChIP-seq- and RNA-seq-based profiling, as well as mutational and biochemical analyses revealed that RpoS-repressed promoters contain a -6G in their respective discriminator sequences; moreover, this -6G proved critical for RpoS to inhibit esrB expression. Mutation of the RpoS R99 residue, an amino acid that molecular modeling predicts interacts with -6G in the esrB discriminator, abolished RpoS' capacity for repression. In a turbot model, an rpoS deletion mutant was attenuated early but not late in infection, whereas a mutant expressing RpoSR99A exhibited elevated fitness throughout the infection period. Collectively, these findings deepen our understanding of how RpoS can inhibit gene expression and demonstrate the temporal variation in the requirement for this sigma factor during infection.
first_indexed 2024-12-19T04:18:36Z
format Article
id doaj.art-3e7f6c2490294fda920b0f07f5f566a2
institution Directory Open Access Journal
issn 1553-7366
1553-7374
language English
last_indexed 2024-12-19T04:18:36Z
publishDate 2018-08-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Pathogens
spelling doaj.art-3e7f6c2490294fda920b0f07f5f566a22022-12-21T20:36:13ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742018-08-01148e100727210.1371/journal.ppat.1007272Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.Kaiyu YinYunpeng GuanRuiqing MaLifan WeiBing LiuXiaohong LiuXiangshan ZhouYue MaYuanxing ZhangMatthew K WaldorQiyao WangEdwardsiella piscicida is a leading fish pathogen that causes significant economic loses in the aquaculture industry. The pathogen depends on type III and type VI secretion systems (T3/T6SS) for growth and virulence in fish and the expression of both systems is controlled by the EsrB transcription activator. Here, we performed a Tn-seq-based screen to uncover factors that govern esrB expression. Unexpectedly, we discovered that RpoS antagonizes esrB expression and thereby inhibits production of E. piscicida's T3/T6SS. Using in vitro transcription assays, we showed that RpoS can block RpoD-mediated transcription of esrB. ChIP-seq- and RNA-seq-based profiling, as well as mutational and biochemical analyses revealed that RpoS-repressed promoters contain a -6G in their respective discriminator sequences; moreover, this -6G proved critical for RpoS to inhibit esrB expression. Mutation of the RpoS R99 residue, an amino acid that molecular modeling predicts interacts with -6G in the esrB discriminator, abolished RpoS' capacity for repression. In a turbot model, an rpoS deletion mutant was attenuated early but not late in infection, whereas a mutant expressing RpoSR99A exhibited elevated fitness throughout the infection period. Collectively, these findings deepen our understanding of how RpoS can inhibit gene expression and demonstrate the temporal variation in the requirement for this sigma factor during infection.http://europepmc.org/articles/PMC6136808?pdf=render
spellingShingle Kaiyu Yin
Yunpeng Guan
Ruiqing Ma
Lifan Wei
Bing Liu
Xiaohong Liu
Xiangshan Zhou
Yue Ma
Yuanxing Zhang
Matthew K Waldor
Qiyao Wang
Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.
PLoS Pathogens
title Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.
title_full Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.
title_fullStr Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.
title_full_unstemmed Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.
title_short Critical role for a promoter discriminator in RpoS control of virulence in Edwardsiella piscicida.
title_sort critical role for a promoter discriminator in rpos control of virulence in edwardsiella piscicida
url http://europepmc.org/articles/PMC6136808?pdf=render
work_keys_str_mv AT kaiyuyin criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT yunpengguan criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT ruiqingma criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT lifanwei criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT bingliu criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT xiaohongliu criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT xiangshanzhou criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT yuema criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT yuanxingzhang criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT matthewkwaldor criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida
AT qiyaowang criticalroleforapromoterdiscriminatorinrposcontrolofvirulenceinedwardsiellapiscicida