The<i>Bacillus subtilis</i>SinR and RapA Developmental Regulators Are Responsible for Inhibition of Spore Development by Alcohol

Gottig, Natalia; Pedrido, María Eugenia; Méndez, Marcelo; Lombardía, Esteban; Rovetto, Adrián J.; Philippe, Valeria; Orsaria, Lelia; Grau, Roberto

doi:10.1128/jb.187.8.2662-2672.2005

Cited by 13 publications

(28 citation statements)

References 43 publications

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“…As indicated earlier, one important requirement for the onset of the sporulation is that sporulation-committed cells induce the expression of spo0A (8,10,23,24,25). Therefore, the level of spo0A expression seems to be a valid tool to determine whether a C. perfringens culture has initiated the formation of spores beyond stage zero.…”

Section: Vol 74 2006 Notes 3653mentioning

confidence: 90%

Inorganic Phosphate Induces Spore Morphogenesis and Enterotoxin Production in the Intestinal Pathogen Clostridium perfringens

et al. 2006

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Clostridium perfringens enterotoxin (CPE) is an important virulence factor for food poisoning and non-food borne gastrointestinal (GI) diseases. Although CPE production is strongly regulated by sporulation, the nature of the signal(s) triggering sporulation remains unknown. Here, we demonstrated that inorganic phosphate (P i ), and not pH, constitutes an environmental signal inducing sporulation and CPE synthesis. In the absence of P i -supplementation, C. perfringens displayed a spo0A phenotype, i.e., absence of polar septation and DNA partitioning in cells that reached the stationary phase of growth. These results received support from our Northern blot analyses which demonstrated that P i was able to counteract the inhibitory effect of glucose at the onset of sporulation and induced spo0A expression, indicating that P i acts as a key signal triggering spore morphogenesis. In addition to being the first study reporting the nature of a physiological signal triggering sporulation in clostridia, these findings have relevance for the development of antisporulation drugs to prevent or treat CPE-mediated GI diseases in humans.Clostridium perfringens is a gram-positive, anaerobic, endospore-forming bacterium causing gastrointestinal and histotoxic infections in humans and animals (2, 6, 9, 17). The virulence of this bacterium largely results from its prolific ability to produce at least 15 different toxins (18). In addition, enterotoxigenic C. perfringens isolates produce a 35-kDa enterotoxin (C. perfringens enterotoxin [CPE]), whose synthesis is under a strict positive control of sporulation (3,5,6,9,17). In C. perfringens, the production of CPE is confined to the large compartment (mother cell) of the sporangium where cpe transcription is believed to be driven from the mother cell-specific forms of the RNA polymerase, RNA-E and RNA-K (30). The copious amount of CPE (as much as 10% or more of the total protein of the developing sporangium) is accumulated probably only in the cytoplasm of the mother cell compartment until its release when the mother cell lyses at the completion of sporulation to liberate the mature spore (17). The released CPE rapidly binds to protein receptors present on the apical surface of enterocytes and induces cell permeabilization with the concomitant appearance of the symptoms of enterotoxaemia, intestinal cramping, and diarrhea (2,17,18).Despite the key role of spores in CPE synthesis and in the dissemination and developing of clostridial diseases, very little is known at the molecular level about the regulatory mechanisms governing the formation of spores in clostridia (6,9,11,13,20,23). Although from genome sequence analyses it can be assumed that the mechanism of spore formation in Bacillus and Clostridium is conserved (21,24,25), the main differences reside at the level of the initiation of the sporulation process (24, 25). While orthologs for spo0A and the genes activated by Spo0AϳP, along with most of the spo genes that are subsequently expressed during the morphogenesis of the spore,...

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Section: Vol 74 2006 Notes 3653mentioning

confidence: 90%

Inorganic Phosphate Induces Spore Morphogenesis and Enterotoxin Production in the Intestinal Pathogen Clostridium perfringens

et al. 2006

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“…For sporulation efficiency, B. subtilis strains were grown in SM for 20 h and then treated with 10% CHCl 3 for 15 min before being plated as previously described (2). Transformation of B. subtilis, to obtain isogenic derivates of the parental strains, was carried out as previously described (18). ␤-Galactosidase assays from B. subtilis strains harboring lacZ fusions were assayed as described previously and the specific activity was expressed in Miller units (2).…”

Section: Methodsmentioning

confidence: 99%

A LuxS-Dependent Cell-to-Cell Language Regulates Social Behavior and Development inBacillus subtilis

et al. 2006

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Cell-to-cell communication in bacteria is mediated by quorum-sensing systems (QSS) that produce chemical signal molecules called autoinducers (AI).In particular, LuxS/AI-2-dependent QSS has been proposed to act as a universal lexicon that mediates intra-and interspecific bacterial behavior. Here we report that the model organism Bacillus subtilis operates a luxS-dependent QSS that regulates its morphogenesis and social behavior. We demonstrated that B. subtilis luxS is a growth-phase-regulated gene that produces active AI-2 able to mediate the interspecific activation of light production in Vibrio harveyi. We demonstrated that in B. subtilis, luxS expression was under the control of a novel AI-2-dependent negative regulatory feedback loop that indicated an important role for AI-2 as a signaling molecule. Even though luxS did not affect spore development, AI-2 production was negatively regulated by the master regulatory proteins of pluricellular behavior, SinR and Spo0A. Interestingly, wild B. subtilis cells, from the undomesticated and probiotic B. subtilis natto strain, required the LuxS-dependent QSS to form robust and differentiated biofilms and also to swarm on solid surfaces. Furthermore, LuxS activity was required for the formation of sophisticated aerial colonies that behaved as giant fruiting bodies where AI-2 production and spore morphogenesis were spatially regulated at different sites of the developing colony. We proposed that LuxS/AI-2 constitutes a novel form of quorumsensing regulation where AI-2 behaves as a morphogen-like molecule that coordinates the social and pluricellular behavior of B. subtilis.Bacteria not only behave as self-sufficient individuals but also act as communities capable of cell-cell communication (7,15,20,42,53). This social interaction leads to the coordination of communitarian activities that resemble, in their complexity, the behaviors observed in multicellular organisms (20,42,49,53,57). This microbial phenomenon is known as quorum sensing, a process by which bacteria monitor their cell population density by measuring the concentration of small secreted signal molecules called autoinducers (57). Even though a vast number of diverse quorum-sensing systems exist (41, 46, 57), they can be divided into two established paradigms that regulate the intraspecific behavior in many bacteria: (i) LuxI/LuxR-type quorum-sensing systems in gram-negative bacteria responsible for the production of N-acyl-L-homoserine lactone autoinducers or type I autoinducers and (ii) oligopeptide/two component-type quorum-sensing circuits in gram-positive bacteria responsible for the production of autoinducer peptides (4,17,26,32,44).However, in recent years, a considerable amount of information has been gained on the existence of another type of quorum-sensing system that not only seems to participate in intraspecific bacterial behavior but also seems to regulate the interspecific interactions among bacteria of different genera. This system involves the production of autoinducer-2 (AI-2) signal molecul...

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“…SinR is a regulator involved in late growth processes and biofilm formation (Kearns et al, 2005). These data suggested that the two regulators RapA and SinR were solely responsible for the observed blockage of sporulation by ethanol stress in the B. subtilis wild type, neither s B nor the general stress genes were considered to be involved in the inhibitory effect of alcohol stress on sporulation (Gottig et al, 2005).…”

Section: Ethanol Stress and Impairment Of Sporulation Specific Transcmentioning

confidence: 99%

Cross‐talk between the general stress response and sporulation initiation in Bacillus subtilis – the σ^B promoter of spo0E represents an AND‐gate

Reder

Albrecht

Gerth

et al. 2012

Environmental Microbiology

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The general stress response and the decision-making processes of sporulation initiation are interconnected pathways in the regulatory network of Bacillus subtilis. In a previous study we provided evidence for a mechanism capable of impairing sporulation by σ(B) -dependent induction of spo0E, encoding a phosphatase specifically inactivating the sporulation master regulator Spo0A~P. Here we show that the σ(B) promoter (Pσ(B)) of spo0E is responsive to sub-inhibitory levels of ethanol stress, producing a σ(B) -dependent sporulation deficient phenotype. In addition to positive regulation by σ(B) , we identified Rok, the repressor of comK, to be a direct repressor of spo0E expression from Pσ(B) . This constellation provides the possibility to integrate signals negatively acting on sporulation initiation through the σ(B) branch as well as a positive feedback loop acting on Pσ(B) by Rok that is most likely a direct consequence of Spo0A~P activity. Thus, the molecular mechanism described here offers the opportunity for cross-talk between the general stress response and sporulation initiation in the adaptational gene expression network of B. subtilis.

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TheBacillus subtilisSinR and RapA Developmental Regulators Are Responsible for Inhibition of Spore Development by Alcohol

Cited by 13 publications

References 43 publications

Inorganic Phosphate Induces Spore Morphogenesis and Enterotoxin Production in the Intestinal Pathogen Clostridium perfringens

Inorganic Phosphate Induces Spore Morphogenesis and Enterotoxin Production in the Intestinal Pathogen Clostridium perfringens

A LuxS-Dependent Cell-to-Cell Language Regulates Social Behavior and Development inBacillus subtilis

Cross‐talk between the general stress response and sporulation initiation in Bacillus subtilis – the σ^B promoter of spo0E represents an AND‐gate

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TheBacillus subtilisSinR and RapA Developmental Regulators Are Responsible for Inhibition of Spore Development by Alcohol

Cited by 13 publications

References 43 publications

Inorganic Phosphate Induces Spore Morphogenesis and Enterotoxin Production in the Intestinal Pathogen Clostridium perfringens

Inorganic Phosphate Induces Spore Morphogenesis and Enterotoxin Production in the Intestinal Pathogen Clostridium perfringens

A LuxS-Dependent Cell-to-Cell Language Regulates Social Behavior and Development inBacillus subtilis

Cross‐talk between the general stress response and sporulation initiation in Bacillus subtilis – the σB promoter of spo0E represents an AND‐gate

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Product

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Cross‐talk between the general stress response and sporulation initiation in Bacillus subtilis – the σ^B promoter of spo0E represents an AND‐gate