Integration of σ
            <sup>B</sup>
            Activity into the Decision-Making Process of Sporulation Initiation in Bacillus subtilis

Reder, Alexander; Gerth, Ulf; Hecker, Michael

doi:10.1128/jb.06490-11

Cited by 31 publications

(52 citation statements)

References 64 publications

(72 reference statements)

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“…Our finding that mutations in rsbU cause sporulation to be temperature sensitive is consistent with interaction between the stress-responsive and sporulation regulatory pathways and supports a model in which activation of SigB interferes with sporulation (15,16).…”

supporting

confidence: 70%

“…It has long been known that addition of ethanol within a 45-min time period around T 1 of sporulation inhibits spore formation (27), presumably through stimulation of the SigB-dependent stress response. More recently, Reder et al (15,16) reported that the spo0E coding sequence is preceded by a perfect SigB promoter sequence and that ectopic expression of SigB interferes with the onset of sporulation. In a construct in which SigB is expressed from a xyloseinducible promoter, addition of xylose leads to overexpression of spo0E.…”

Section: Discussionmentioning

confidence: 99%

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A Mutation in the Bacillus subtilis rsbU Gene That Limits RNA Synthesis during Sporulation

et al. 2017

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Mutants of Bacillis subtilis that are temperature sensitive for RNA synthesis during sporulation were isolated after selection with a 32 P suicide agent. Whole-genome sequencing revealed that two of the mutants carried an identical lesion in the rsbU gene, which encodes a phosphatase that indirectly activates SigB, the stress-responsive RNA polymerase sigma factor. The mutation appeared to cause RsbU to be hyperactive, because the mutants were more resistant than the parent strain to ethanol stress. In support of this hypothesis, pseudorevertants that regained wild-type levels of sporulation at high temperature had secondary mutations that prevented expression of the mutant rsbU gene. The properties of these RsbU mutants support the idea that activation of SigB diminishes the bacterium's ability to sporulate.IMPORTANCE Most bacterial species encode multiple RNA polymerase promoter recognition subunits (sigma factors). Each sigma factor directs RNA polymerase to different sets of genes; each gene set typically encodes proteins important for responses to specific environmental conditions, such as changes in temperature, salt concentration, and nutrient availability. A selection for mutants of Bacillus subtilis that are temperature sensitive for RNA synthesis during sporulation unexpectedly yielded strains with a point mutation in rsbU, a gene that encodes a protein that normally activates sigma factor B (SigB) under conditions of salt stress. The mutation appears to cause RsbU, and therefore SigB, to be active inappropriately, thereby inhibiting, directly or indirectly, the ability of the cells to transcribe sporulation genes.KEYWORDS sigma factor B, RsbU, Bacillus subtilis, sporulation S porulation is an elaborate developmental process involving the significant change in expression of nearly 600 genes in Bacillus subtilis, representing more than 10% of its genome (1). There are at least five RNA polymerase sigma factors (promoter recognition proteins) that mediate this complex change in gene expression. During the formation of the metabolically dormant endospore, two of these sigma factors are active in the forespore (SigF and SigG) and two in the mother cell (SigE and SigK) (2).The decision to undergo sporulation in response to nutrient deprivation is made in the first 2 h after B. subtilis enters the stationary phase. After that time, the cell becomes committed to completing the ordered sporulation program. Spo0A, the master regulator governing the decision to sporulate (3,4), is activated by phosphorylation carried out by a phosphorelay system involving five kinases and two phosphorelay proteins, Spo0B and Spo0F (5). Only the active phosphorylated Spo0A form (Spo0AϳP) directly contacts promoters, resulting in the induction of some genes and the repression of others. Under some conditions, Spo0AϳP is subject to inactivation by dephosphorylation by the dedicated phosphatase, Spo0E (4, 5).In 1973, before any of the sporulation sigma factors had been discovered, we

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confidence: 70%

Section: Discussionmentioning

confidence: 99%

A Mutation in the Bacillus subtilis rsbU Gene That Limits RNA Synthesis during Sporulation

et al. 2017

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“…and B of endosporulators, which are both involved in the stress response (70). Importantly, B of B. subtilis is not required for sporulation, although B -inducing signals can influence activation of Spo0A (71).…”

Section: Resultsmentioning

confidence: 99%

A Genomic Signature and the Identification of New Sporulation Genes

et al. 2013

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Bacterial endospores are the most resistant cell type known to humans, as they are able to withstand extremes of temperature, pressure, chemical injury, and time. They are also of interest because the endospore is the infective particle in a variety of human and livestock diseases. Endosporulation is characterized by the morphogenesis of an endospore within a mother cell. Based on the genes known to be involved in endosporulation in the model organism Bacillus subtilis, a conserved core of about 100 genes was derived, representing the minimal machinery for endosporulation. The core was used to define a genomic signature of about 50 genes that are able to distinguish endospore-forming organisms, based on complete genome sequences, and we show this 50-gene signature is robust against phylogenetic proximity and other artifacts. This signature includes previously uncharacterized genes that we can now show are important for sporulation in B. subtilis and/or are under developmental control, thus further validating this genomic signature. We also predict that a series of polyextremophylic organisms, as well as several gut bacteria, are able to form endospores, and we identified 3 new loci essential for sporulation in B. subtilis: ytaF, ylmC, and ylzA. In all, the results support the view that endosporulation likely evolved once, at the base of the Firmicutes phylum, and is unrelated to other bacterial cell differentiation programs and that this involved the evolution of new genes and functions, as well as the cooption of ancestral, housekeeping functions. Bacterial endospores, such as those formed by species of the Bacillus and Clostridium genera, are arguably the most resistant cellular structures known to scientists. Endospores resist physical and chemical changes, such as exposure to solvents, oxidizing agents, and lytic enzymes, high temperatures, vacuum, acceleration, and irradiation, that would rapidly destroy the vegetative form of the bacterium (1-3). The extreme conditions endured by bacterial endospores include simulated and actual extraterrestrial environments (2). The resilience of the endospore allows it to remain viable in the environment for long periods of time, contributing to the wide geographic distributions of spores in Earth's ecosystems (2). It also allows endospore formers to occupy niches in the gastrointestinal (GI) tract of metazoans, establishing either symbiotic or commensal relationships or pathogenic interactions, in which case the spore often serves as the infectious vehicle (4-7). The robustness of endospores is also the basis for several applications of endospores in biomedicine and biotechnology, including their use in probiotic formulations or as platforms for the display of enzymes or antigens (8-10).Most of the previously described endosporulating bacteria belong to the Clostridia (anaerobic) and Bacilli (aerobic) classes of the Firmicutes phylum, one of the two eubacterial phyla that groups Gram-positive organisms (11). However, endospore formers are found in other classes within t...

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“…A gene encoding a homolog for the sporulation sigma factor SigK of bacilli is present in the genome of C. botulinum ATCC 3502 (open reading frame [ORF] CBO2541) (11) and was recently shown to be essential in early stage sporulation in C. botulinum (12) and in Clostridium perfringens (13,14) and putatively in transcriptional activation of the sporulation master switch Spo0A of C. botulinum (12). In B. subtilis, recent findings suggest an interesting interconnection between the decision to sporulate and adaptation to stress as nongrowing "vegetative dormant" cells (15,16). These observations propose a role for the stress sigma factor SigB in regulating the activity of Spo0A of B. subtilis.…”

mentioning

confidence: 99%

“…These observations propose a role for the stress sigma factor SigB in regulating the activity of Spo0A of B. subtilis. The lack of sigB in the C. botulinum ATCC 3502 genome suggests that the network for decision making between sporulation initiation and stress adaptation of this organism is regulated differently from the one proposed for B. subtilis (15,16). We thus sought to investigate the behavior and role of the alternative sigma factor SigK in response to stress in C. botulinum ATCC 3502.…”

mentioning

confidence: 99%

Alternative Sigma Factor SigK Has a Role in Stress Tolerance of Group I Clostridium botulinum Strain ATCC 3502

Dahlsten

Kirk

Lindström

et al. 2013

Appl Environ Microbiol

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The role of the alternative sigma factor SigK in cold and osmotic stress tolerance of Clostridium botulinum ATCC 3502 was demonstrated by induction of sigK after temperature downshift and exposure to hyperosmotic conditions and by impaired growth of the sigK mutants under the respective conditions. T he ability of the anaerobic, Gram-positive, spore-forming, food-borne pathogen Clostridium botulinum to survive, grow, and subsequently produce botulinum neurotoxin in foods (1) raises substantial concern over food safety (2, 3). In minimally processed foods, the extrinsic and intrinsic hurdles used to control the outgrowth and toxin production by C. botulinum include refrigeration, heat treatment, increased osmolarity or low water activity, extreme pH, and preservatives (2, 4). Understanding the mechanisms by which food-borne pathogenic bacteria cope with these stress conditions is of key importance in designing modern food safety measures.Sigma factors are dissociable RNA polymerase subunits that alter the promoter specificity of the RNA polymerase complex under different environmental and growth phase-dependent conditions. A stress-responsive alternative sigma factor, SigB, has been identified (5-8) and has been shown to play a role in cold adaptation of Listeria monocytogenes (9) and Bacillus subtilis (10). However, the genome of C. botulinum ATCC 3502 does not harbor a homolog for sigB (11), suggesting mechanisms of general stress response different from those in the Gram-positive model organism B. subtilis. A gene encoding a homolog for the sporulation sigma factor SigK of bacilli is present in the genome of C. botulinum ATCC 3502 (open reading frame [ORF] CBO2541) (11) and was recently shown to be essential in early stage sporulation in C. botulinum (12) and in Clostridium perfringens (13,14) and putatively in transcriptional activation of the sporulation master switch Spo0A of C. botulinum (12). In B. subtilis, recent findings suggest an interesting interconnection between the decision to sporulate and adaptation to stress as nongrowing "vegetative dormant" cells (15,16). These observations propose a role for the stress sigma factor SigB in regulating the activity of Spo0A of B. subtilis. The lack of sigB in the C. botulinum ATCC 3502 genome suggests that the network for decision making between sporulation initiation and stress adaptation of this organism is regulated differently from the one proposed for B. subtilis (15,16). We thus sought to investigate the behavior and role of the alternative sigma factor SigK in response to stress in C. botulinum ATCC 3502.The C. botulinum ATCC 3502 wild-type strain was evaluated for relative sigK expression levels after cold shock, exposure to hyperosmotic conditions, exposure to acidity, or under optimal growth conditions, using quantitative reverse transcription-PCR (primers sigK-qPCR-F [5=-ACTTATGGGATGTACTAGGAAGT G-3=] and sigK-qPCR-R [5=-TTCTTCTTCATCACTTAGAGGCT TG-3=]) (17-19) and the Pfaffl method (20) for quantitation, with 16S rrn expression as a normalization re...

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Integration of σ ^B Activity into the Decision-Making Process of Sporulation Initiation in Bacillus subtilis

Cited by 31 publications

References 64 publications

A Mutation in the Bacillus subtilis rsbU Gene That Limits RNA Synthesis during Sporulation

A Mutation in the Bacillus subtilis rsbU Gene That Limits RNA Synthesis during Sporulation

A Genomic Signature and the Identification of New Sporulation Genes

Alternative Sigma Factor SigK Has a Role in Stress Tolerance of Group I Clostridium botulinum Strain ATCC 3502

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Integration of σ B Activity into the Decision-Making Process of Sporulation Initiation in Bacillus subtilis

Cited by 31 publications

References 64 publications

A Mutation in the Bacillus subtilis rsbU Gene That Limits RNA Synthesis during Sporulation

A Mutation in the Bacillus subtilis rsbU Gene That Limits RNA Synthesis during Sporulation

A Genomic Signature and the Identification of New Sporulation Genes

Alternative Sigma Factor SigK Has a Role in Stress Tolerance of Group I Clostridium botulinum Strain ATCC 3502

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Integration of σ ^B Activity into the Decision-Making Process of Sporulation Initiation in Bacillus subtilis