Conserved and Variable Functions of the σE Stress Response in Related Genomes

Rhodius, Virgil A.; Suh, Won Chul; Nonaka, Gen; West, Joyce F.; Gross, Carol A.

doi:10.1371/journal.pbio.0040002

Cited by 485 publications

(696 citation statements)

References 94 publications

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“…Among them, the presence of rpoE1 suggests an autoregulation, as described in Escherichia coli and other bacteria (Rhodius et al, 2006). In Caulobacter crescentus, Sinorhizobium meliloti, Rhizobium etli and Bradyrhizobium japonicum, the rpoE1 homologues (sigT, rpoE2, rpoE4 and ecfG, respectively) are positively autoregulated ( Finally, TEM experiments indicated that the flagellum is longer in DrpoE1 than the wild-type strain.…”

Section: Discussionmentioning

confidence: 80%

RpoE1, an extracytoplasmic function sigma factor, is a repressor of the flagellar system in Brucella melitensis

et al. 2011

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RpoE1, an extracytoplasmic function sigma factor, is a repressor of the flagellar system in Brucella melitensis Unité de Recherche en Biologie Molé culaire (URBM), Faculté s Universitaires Notre-Dame de la Paix Namur (FUNDP), 61 rue de Bruxelles, B-5000 Namur, BelgiumThe genome of Brucella melitensis contains genes coding for the sigma factors RpoD, RpoN, RpoH1, RpoH2, RpoE1 and RpoE2. Previously published data show that B. melitensis is flagellated and that an rpoE1 mutant overexpresses the flagellar protein FlgE. In this study, we demonstrate that mutation of rpoE1 causes an overexpression of the flagellar genes fliF, flgE, fliC, flaF and flbT, correlating with the production of a longer filament and thereby demonstrating that RpoE1 acts as a flagellar repressor. Moreover, mutation of rpoE1 increases the promoter activity of the flagellar master regulator ftcR, suggesting that RpoE1 acts upstream of ftcR. Together, these data show that RpoE1 represses the flagellar synthesis and filament length in B. melitensis. INTRODUCTIONBrucellae are Gram-negative, intracellular pathogenic bacteria that cause brucellosis in a variety of mammals, including humans. For a long time, they were considered as being unflagellated. However, a sheathed flagellum has recently been discovered in Brucella melitensis and flagellar mutants are found to be impaired for infection in vivo (Ferooz & Letesson, 2010;Fretin et al., 2005;Zygmunt et al., 2006).The bacterial flagellum is a complex organelle used for motility and consists of at least three structural elements, the basal body, the hook and the filament (Macnab, 1999). The basal body, working as a motor, is embedded within the cell envelope and is anchored in the cytoplasmic membrane via the MS-ring structure, while the hook and filament, which function as a universal joint and a propeller, respectively, extend outwards from the cells (Minamino et al., 2008).Sigma and anti-sigma factors play important roles in the regulation of the flagellar genes (Smith & Hoover, 2009). The genome of B. melitensis has revealed the presence of genes encoding six sigma factors (rpoD, rpoH1, rpoH2, rpoE1, rpoE2 and rpoN) (Delory et al., 2006). The rpoD gene encodes the housekeeping sigma factor, the rpoH1 and rpoH2 genes encode two s 32 homologues, rpoE1 and rpoE2 encode two extracytoplasmic function (ECF) sigma factors and the rpoN gene encodes a s 54 homologue. The phenotypic characterizations were done on the five nonessential sigma factor mutants DrpoH1, DrpoH2, DrpoE1, DrpoE2 and DrpoN (Delory et al., 2006). Interestingly, at early growth phase in rich liquid medium, DrpoE1 overproduces the flagellar hook protein FlgE, suggesting that the flagellar system synthesis could be downregulated by the ECF sigma factor RpoE1 in B. melitensis (Delory et al., 2006).In this study, we demonstrate that the ECF sigma factor RpoE1 is a flagellar repressor in B. melitensis and that RpoE1 controls the length of the flagellar filament. METHODSBacterial strains and culture conditions. All strains and plasmids used ...

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Section: Discussionmentioning

confidence: 80%

RpoE1, an extracytoplasmic function sigma factor, is a repressor of the flagellar system in Brucella melitensis

et al. 2011

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“…At the same time numerous omp mRNAs, which are major targets of σ Eactivated sRNAs (Rhodius et al, 2006), were rapidly down-regulated. It is tempting to speculate that activation of the σ E response and the resulting suppression of multiple outer membrane proteins might represent another immune evasion strategy of Salmonella.…”

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confidence: 99%

Dual RNA-seq of pathogen and host

2012

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SummaryThe infection of a eukaryotic host cell by a bacterial pathogen is one of the most intimate examples of cross-kingdom interactions in biology. Infection processes are highly relevant from both a basic research as well as a clinical point of view. Sophisticated mechanisms have evolved in the pathogen to manipulate the host response and vice versa host cells have developed a wide range of anti-microbial defense strategies to combat bacterial invasion and clear infections.However, it is this diversity and complexity that makes infection research so challenging to technically address as common approaches have either been optimized for bacterial or eukaryotic organisms. Instead, methods are required that are able to deal with the often dramatic discrepancy between host and pathogen with respect to various cellular properties and processes. One class of cellular macromolecules that exemplify this host-pathogen heterogeneity is given by their transcriptomes: Bacterial transcripts differ from their eukaryotic counterparts in many aspects that involve both quantitative and qualitative traits. The entity of RNA transcripts present in a cell is of paramount interest as it reflects the cell's physiological state under the given condition. Genome-wide transcriptomic techniques such as RNA-seq have therefore been used for single-organism analyses for several years, but their applicability has been limited for infection studies.The present work describes the establishment of a novel transcriptomic approach for infection biology which we have termed "Dual RNA-seq". Using this technology, it was intended to shed light particularly on the contribution of non-protein-encoding transcripts to virulence, as these classes have mostly evaded previous infection studies due to the lack of suitable methods. The performance of Dual RNA-seq was evaluated in an in vitro infection model based on the important facultative intracellular pathogen Salmonella enterica serovar Typhimurium and different human cell lines. Dual RNA-seq was found to be capable of capturing all major bacterial and human transcript classes and proved reproducible. During the course of these experiments, a previously largely uncharacterized bacterial small non-coding RNA (sRNA), referred to as STnc440, was identified as one of the most strongly induced genes in intracellular Salmonella.Interestingly, while inhibition of STnc440 expression has been previously shown to cause a virulence defect in different animal models of Salmonellosis, the underlying molecular mechanisms have remained obscure. Here, classical genetics, transcriptomics and biochemical assays proposed a complex model of Salmonella gene expression control that is orchestrated by this sRNA. In particular, STnc440 was found to be involved in the regulation of multiple bacterial target mRNAs by direct base pair interaction with consequences for Salmonella virulence and

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“…These unassembled proteins are sensed in the periplasm leading to activation of the alternative sigma factor (SigmaE), which resides in the cytoplasm (36,39). SigmaE then binds to RNA polymerase core selectively promoting the transcription of genes in its regulon, such as periplasmic located chaperones, folding catalysts, proteases, and factors involved in lipid biogenesis as well as small RNA regulators (40,41). Collectively, the upregulation of these factors acts to re-establish protein homeostasis and envelope integrity.…”

Section: Proteolytic Control Of the Envelope Stress Response In E Colimentioning

confidence: 99%

“…Collectively, the upregulation of these factors acts to re-establish protein homeostasis and envelope integrity. For example, the periplasmic protein DegP is upregulated on envelope stress and undergoes oligomerization and activation in the presence of unfolded protein, assisting the removal of the damaged proteins by repair or proteolysis (40,42,43). So how is the unfolded protein stress signal sensed and transmitted across the membrane?…”

Section: Proteolytic Control Of the Envelope Stress Response In E Colimentioning

confidence: 99%

Unfolded protein responses in bacteria and mitochondria: A central role for the ClpXP machine

2011

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SummaryIn the crowded environment of a cell, the protein quality control machinery, such as molecular chaperones and proteases, maintains a population of folded and hence functional proteins. The accumulation of unfolded proteins in a cell is particularly harmful as it not only reduces the concentration of active proteins but also overburdens the protein quality control machinery, which in turn, can lead to a significant increase in nonproductive folding and protein aggregation. To circumvent this problem, cells use heat shock and unfolded protein stress response pathways, which essentially sense the change to protein homeostasis upregulating protein quality control factors that act to restore the balance. Interestingly, several stress response pathways are proteolytically controlled. In this review, we provide a brief summary of targeted protein degradation by AAA1 proteases and focus on the role of ClpXP proteases, particularly in the signaling pathway of the Escherichia coli extracellular stress response and the mitochondrial unfolded protein response. IUBMBIUBMB Life, 63(11): 955-963, 2011

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Conserved and Variable Functions of the σE Stress Response in Related Genomes

Cited by 485 publications

References 94 publications

RpoE1, an extracytoplasmic function sigma factor, is a repressor of the flagellar system in Brucella melitensis

RpoE1, an extracytoplasmic function sigma factor, is a repressor of the flagellar system in Brucella melitensis

Dual RNA-seq of pathogen and host

Unfolded protein responses in bacteria and mitochondria: A central role for the ClpXP machine

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