Genetic Dissection of the Sporulation Protein SpoIIE and Its Role in Asymmetric Division in<i>Bacillus subtilis</i>

Carniol, Karen; Ben-Yehuda, Sigal; King, Nicole; Losick, Richard

doi:10.1128/jb.187.10.3511-3520.2005

Cited by 43 publications

(50 citation statements)

References 39 publications

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“…It is possible that other important elements required for the proper activation of F , including the instability of the protein and transient genetic asymmetry (the exclusion of spoIIAB from the forespore at an early stage in chromosome segregation) (132,133) have also been conserved. SpoIIE also promotes polar septum formation, a function that requires its phosphatase domain (although not its catalytic activity) (131), and that may also have been conserved.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

confidence: 99%

A Genomic Signature and the Identification of New Sporulation Genes

et al. 2013

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“…This proposed role is consistent with the topology of DivIB in the membrane, with the functional C-terminal bulk of the protein being accessible to the cell wall (22,26). The only other protein that, when absent in B. subtilis, forms a thick polar septa is SpoIIE, a bifunctional protein critical for polar cell division in this organism (7,29). SpoIIE is unique in that it is the only protein known to be required for polar septation but not for vegetative symmetric division, raising the possibility that it too is involved in the modification of polar septal peptidoglycan (3,25).…”

Section: Discussionmentioning

confidence: 99%

Requirement for the Cell Division Protein DivIB in Polar Cell Division and Engulfment during Sporulation inBacillus subtilis

et al. 2006

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During spore formation in Bacillus subtilis, cell division occurs at the cell pole and is believed to require essentially the same division machinery as vegetative division. Intriguingly, although the cell division protein DivIB is not required for vegetative division at low temperatures, it is essential for efficient sporulation under these conditions. We show here that at low temperatures in the absence of DivIB, formation of the polar septum during sporulation is delayed and less efficient. Furthermore, the polar septa that are complete are abnormally thick, containing more peptidoglycan than a normal polar septum. These results show that DivIB is specifically required for the efficient and correct formation of a polar septum. This suggests that DivIB is required for the modification of sporulation septal peptidoglycan, raising the possibility that DivIB either regulates hydrolysis of polar septal peptidoglycan or is a hydrolase itself. We also show that, despite the significant number of completed polar septa that form in this mutant, it is unable to undergo engulfment. Instead, hydrolysis of the peptidoglycan within the polar septum, which occurs during the early stages of engulfment, is incomplete, producing a similar phenotype to that of mutants defective in the production of sporulation-specific septal peptidoglycan hydrolases. We propose a role for DivIB in sporulation-specific peptidoglycan remodelling or its regulation during polar septation and engulfment.

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“…2). Specifically, we examined spoIIE, which encodes one of the first sporulation-specific proteins to be induced (8,38), spo0A, encoding a master regulator that controls the initiation of several developmental programs, including endospore formation, matrix production, and competence (9), and kinA, whose product is primarily responsible for the phosphorylation of Spo0A (39). For comparison we also examined glnA, which encodes glutamine synthetase and is not expected to change during the timing examined here (40).…”

Section: Cells Lacking 6s-1 Rna Have Altered Timing Of Sporulationmentioning

confidence: 99%

6S-1 RNA Function Leads to a Delay in Sporulation in Bacillus subtilis

Cavanagh

Wassarman

2013

J Bacteriol

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We have discovered that 6S-1 RNA (encoded by bsrA) is important for appropriate timing of sporulation in Bacillus subtilis in that cells lacking 6S-1 RNA sporulate earlier than wild-type cells. The time to generate a mature spore once the decision to sporulate has been made is unaffected by 6S-1 RNA, and, therefore, we propose that it is the timing of onset of sporulation that is altered. Interestingly, the presence of cells lacking 6S-1 RNA in coculture leads to all cell types exhibiting an early-sporulation phenotype. We propose that cells lacking 6S-1 RNA modify their environment in a manner that promotes early sporulation. In support of this model, resuspension of wild-type cells in conditioned medium from ⌬bsrA cultures also resulted in early sporulation. Use of Escherichia coli growth as a reporter of the nutritional status of conditioned media suggested that B. subtilis cells lacking 6S-1 RNA reduce the nutrient content of their environment earlier than wild-type cells. Several pathways known to impact the timing of sporulation, such as the skf-and sdp-dependent cannibalism pathways, were eliminated as potential targets of 6S-1 RNA-mediated changes, suggesting that 6S-1 RNA activity defines a novel mechanism for altering the timing of onset of sporulation. In addition, 6S-2 RNA does not influence the timing of sporulation, providing further evidence of the independent influences of these two related RNAs on cell physiology.

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Genetic Dissection of the Sporulation Protein SpoIIE and Its Role in Asymmetric Division inBacillus subtilis

Cited by 43 publications

References 39 publications

A Genomic Signature and the Identification of New Sporulation Genes

A Genomic Signature and the Identification of New Sporulation Genes

Requirement for the Cell Division Protein DivIB in Polar Cell Division and Engulfment during Sporulation inBacillus subtilis

6S-1 RNA Function Leads to a Delay in Sporulation in Bacillus subtilis

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