Complex transcriptional regulation of citrate metabolism in Clostridium perfringens

Yuan, Yonghui; Ohtani, Kaori; Yoshizawa, Satoko; Shimizu, Tohru

doi:10.1016/j.anaerobe.2011.09.004

Cited by 11 publications

(5 citation statements)

References 32 publications

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“…Our data suggest that the BsaR/BsaS two-component system is required for P sipW expression. bsaRS is reported to be involved in the expression of citrate metabolism genes 45 . This result implies that extracellular citrate influences sipW-bsaABCRSD operon expression.…”

Section: Discussionmentioning

confidence: 99%

Temperature-regulated heterogeneous extracellular matrix gene expression defines biofilm morphology in Clostridium perfringens

Obana

Nakamura

Nomura

2020

npj Biofilms Microbiomes

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Cells in biofilms dynamically adapt to surrounding environmental conditions, which alters biofilm architecture. The obligate anaerobic pathogen Clostridium perfringens shows different biofilm structures in different temperatures. Here we find that the temperature-regulated production of extracellular polymeric substance (EPS) is necessary for morphological changes in biofilms. We identify BsaA proteins as an EPS matrix necessary for pellicle biofilm formation at lower temperature and find that extracellularly secreted BsaA protein forms filamentous polymers. We show that sipW-bsaA operon expression is bimodal, and the EPS-producing population size is increased at a lower temperature. This heterogeneous expression of the EPS gene requires a two-component system. We find that EPS-producing cells cover EPS-nonproducing cells attaching to the bottom surface. In the deletion mutant of pilA2, encoding a type IV pilin, the EPS gene expression is ON in the whole population. This heterogeneity is further regulated by the cleavage of the pilA2 mRNA by RNase Y, causing temperature-responsive EPS expression in biofilms. As temperature is an environmental cue, C. perfringens may modulate EPS expression to induce morphological changes in biofilm structure as a strategy for adapting to interhost and external environments.

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Section: Discussionmentioning

confidence: 99%

Temperature-regulated heterogeneous extracellular matrix gene expression defines biofilm morphology in Clostridium perfringens

Obana

Nakamura

Nomura

2020

npj Biofilms Microbiomes

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“…According to our transcriptome analysis, a number of mRNAs accumulated under RNase Y-depleted conditions, suggesting these mRNAs are direct targets for degradation by RNase Y (Table S2). To analyze the effects of RNase Y on mRNA half-life, we selected the following genes that accumulated when RNase Y was depleted: spo0A, encoding a sporulation master regulator (24); monocistronic nagK, encoding the -toxin hyaluronidase (25); the tetracistronic operon ycgJ-metB-cysK-luxS, encoding the AI-2-producing enzyme LuxS (26); and the long operon CPE0514-CPE0520, which encodes putative extracellular proteins and the two-component system (27). The monocistronic spo0A and nagK mRNAs were highly stable under RNase Y-depleted conditions, although they were rapidly degraded after the addition of rifampin in the presence of the inducer lactose ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Role of RNase Y in Clostridium perfringens mRNA Decay and Processing

2017

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RNase Y is a major endoribonuclease that plays a crucial role in mRNA degradation and processing. We study the role of RNase Y in the Gram-positive anaerobic pathogen Clostridium perfringens, which until now has not been well understood. Our study implies an important role for RNase Y-mediated RNA degradation and processing in virulence gene expression and the physiological development of the organism. We began by constructing an RNase Y conditional knockdown strain in order to observe the importance of RNase Y on growth and virulence. Our resulting transcriptome analysis shows that RNase Y affects the expression of many genes, including toxin-producing genes. We provide data to show that RNase Y depletion repressed several toxin genes in C. perfringens and involved the virR-virS twocomponent system. We also observe evidence that RNase Y is indispensable for processing and stabilizing the transcripts of colA (encoding a major toxin collagenase) and pilA2 (encoding a major pilin component of the type IV pili). Posttranscriptional regulation of colA is known to be mediated by cleavage in the 5= untranslated region (5=UTR), and we observe that RNase Y depletion diminishes colA 5=UTR processing. We show that RNase Y is also involved in the posttranscriptional stabilization of pilA2 mRNA, which is thought to be important for host cell adherence and biofilm formation.IMPORTANCE RNases have important roles in RNA degradation and turnover in all organisms. C. perfringens is a Gram-positive anaerobic spore-forming bacterial pathogen that produces numerous extracellular enzymes and toxins, and it is linked to digestive disorders and disease. A highly conserved endoribonuclease, RNase Y, affects the expression of hundreds of genes, including toxin genes, and studying these effects is useful for understanding C. perfringens specifically and RNases generally. Moreover, RNase Y is involved in processing specific transcripts, and we observed that this processing in C. perfringens results in the stabilization of mRNAs encoding a toxin and bacterial extracellular apparatus pili. Our study shows that RNase activity is associated with gene expression, helping to determine the growth, proliferation, and virulence of C. perfringens.

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“…40 Of those TCRS, most have received little study except for VirS/VirR. This TCRS, encoded by the virS/ No known association with human disease; suspected, but not confirmed association with gastrointestinal disease of cattle, sheep and rabbits.…”

Section: Introduction To the Virs/virr And Agr-like C Perfringens Rementioning

confidence: 99%

Host cell-induced signaling causesClostridium perfringensto upregulate production of toxins important for intestinal infections

Chen

Uzal

et al. 2013

Gut Microbes

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These authors contributed equally to this work.Keywords: Clostridium perfringens, enterotoxin, beta toxin, epsilon toxin, quorum sensing, Agr, two component regulatory system, VirS/VirR, intestinal infectionClostridium perfringens causes enteritis and enterotoxemia in humans and livestock due to prolific toxin production. In broth culture, C. perfringens uses the agr-like quorum sensing (QS) system to regulate production of toxins important for enteritis/ enterotoxemia, including beta toxin (cPB), enterotoxin, and epsilon toxin (eTX). The VirS/Virr two-component regulatory system (TcrS) also controls cPB production in broth cultures. Both the agr-like QS and VirS/Virr systems are important when C. perfringens senses enterocyte-like caco-2 cells and responds by upregulating cPB production; however, only the agr-like QS system is needed for host cell-induced eTX production. These in vitro observations have pathophysiologic relevance since both the VirS/Virr and agr-like QS signaling systems are required for C. perfringens strain cN3685 to produce cPB in vivo and to cause enteritis or enterotoxemia. Thus, apparently upon sensing its presence in the intestines, C. perfringens utilizes QS and TcrS signaling to produce toxins necessary for intestinal virulence.

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Complex transcriptional regulation of citrate metabolism in Clostridium perfringens

Cited by 11 publications

References 32 publications

Temperature-regulated heterogeneous extracellular matrix gene expression defines biofilm morphology in Clostridium perfringens

Temperature-regulated heterogeneous extracellular matrix gene expression defines biofilm morphology in Clostridium perfringens

Role of RNase Y in Clostridium perfringens mRNA Decay and Processing

Host cell-induced signaling causesClostridium perfringensto upregulate production of toxins important for intestinal infections

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