The Relationship Between DNA Replication and the Induction of Sporulation in Bacillus subtilis

Dunn, G.; Jeffs, Peter W.; Mann, Nicholas H.; Torgersen, Dawn; Young, Michael

doi:10.1099/00221287-108-2-189

Cited by 38 publications

(39 citation statements)

References 22 publications

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“…A detailed sequence of cell cycle events has been deduced for the abrupt transition from growth to sporulation by using the classical resuspension method (42). In addition to providing a picture of the changes in cell size and DNA content that occur as cells initiate sporulation, the results confirm that there is a period of sensitivity in the cell cycle during which cells can respond to a starvation stimulus and switch to asymmetric division (7,11,29). This point of sensitivity need not, as previously assumed, correspond to a stage within the DNA replication cycle.…”

mentioning

confidence: 88%

“…This could obviously be a consequence of sister cells being synchronized with respect to the cell cycle, having been the products of the same division. Secondly, experiments with inhibitors of DNA replication suggested that cells could initiate sporulation only at a particular point in the DNA replication cycle (7,11,29). However, the other cell cycle parameters of cells at the postulated sensitive stage (e.g., mass and length) have not been further investigated.…”

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confidence: 99%

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Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis

Hauser

Errington

1995

J Bacteriol

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To elucidate the process of asymmetric division during sporulation of Bacillus subtilis, we have measured changes in cell cycle parameters during the transition from vegetative growth to sporulation. Because the propensity of B. subtilis to grow in chains of cells precludes the use of automated cell-scanning devices, we have developed a fluorescence microscopic method for analyzing cell cycle parameters in individual cells. From the results obtained, and measurements of DNA replication fork elongation rates and the escape time of sporulation from the inhibition of DNA replication, we have derived a detailed time scale for the early morphological events of sporulation which is mainly consistent with the cell cycle changes expected following nutritional downshift. The previously postulated sensitive stage in the DNA replication cycle, beyond which the cell is unable to sporulate without a new cell cycle, could represent a point in the division cycle at which the starved cell cannot avoid attaining the initiation mass for DNA replication and thus embarking on another round of the cell cycle. The final cell cycle event, formation of the asymmetric spore septum, occurs at about the time in the cell cycle at which the uninduced cell would have divided centrally, in keeping with the view that spore septation is a modified version of vegetative division.Under starvation conditions, Bacillus subtilis undergoes a differentiation process that culminates with the release of a dormant endospore. The first overt morphological event in this process is the formation of a polar division septum positioned quite differently from the centrally located septum of the vegetative cell. Asymmetric septation generates two compartments of unequal size, a large one, the mother cell, and a smaller one, the prespore. The morphology of cells during the asymmetric division process (20, 21) and the common requirements for cell division genes, such as ftsZ (4), divIC (27), and divIB (3), suggest that spore septum formation is a modified form of vegetative division.Although a great deal is known about the nature of the nutritional signals controlling the switch from vegetative growth to sporulation (22) and about the changes in transcription that accompany and direct the differentiation of prespore and mother cell (15), little is known about how the cell cycle is modified at the onset of sporulation. The starting material for sporulation is apparently a cell containing two fully replicated chromosomes, one destined for the spore and the other remaining in the mother cell (2,19,37,41,46). Consequently, when sporulation is initiated after a period of relatively rapid growth and thus dichotomous replication, the cell must undergo a complex transition to a state in which two completed, nonreplicating chromosomes are present. In order for this to occur, it seems likely that ongoing rounds of replication must be completed and new rounds avoided, but how this reorganization of the cell cycle is achieved has not been elucidated.Two lines of evidence, obt...

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confidence: 88%

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confidence: 99%

Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis

Hauser

Errington

1995

J Bacteriol

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“…For cells to initiate the process of sporulation, they must be starved for a carbon, nitrogen, or phosphorus source (Sonenshein 1989), and be at a relatively high density (Grossman and Losick 1988). Spore formation also requires DNA replication (Dunn et al 1978;Shibano et al 1978;Ireton and Grossman 1992), and blocking DNA synthesis affects the ability of cells to enter into the earliest stages of sporulation (Ireton and Grossman 1992).…”

Section: Mutations In Spo0a That Bypass Developmental Signalsmentioning

confidence: 99%

“…Starvation for a carbon, nitrogen, or phosphorus source is the primary signal needed to initiate spore formation (Sonenshein 1989). In addition, cells must be at a relatively high density (Grossman and Losick 19881 and undergoing DNA synthesis (Dunn et al 1978;Shibano et al 1978;Ireton and Grossman 1992) for spore formation to begin. All three of these conditions must be met for the successful initiation of sporulation, and B. subtilis must have mechanisms for sensing and integrating these signals to ensure the appropriate developmental response.…”

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Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor.

Ireton¹,

Rudner²,

Siranosian³

et al. 1993

Genes Dev.

247

221

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Multiple physiological and environmental signals are needed to initiate endospore formation in Bacillus subtilis. One key event controlling sporulation is activation of the Spo0A transcription factor. Spo0A is a member of a large family of conserved regulatory proteins whose activity is controlled by phosphorylation. We have isolated deletion mutations that remove part of the conserved amino terminus of Spo0A and make the transcription factor constitutively active, indicating that the amino terminus normally functions to keep the protein in an inactive state. Expression of an activated gene product is sufficient to activate expression of several sporulation genes in the absence of signals normally needed for initiation of sporulation. Our results indicate that nutritional, cell density, and cell-cycle signals are integrated through the phosphorylation pathway that controls activation of Spo0A.

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“…They showed that there is a sensitive period in the cell cycle during which sporulation can be initiated. Once cells pass this window of opportunity, they must traverse another cycle before being capable of initiation, irrespective of their nutritional status (Dawes et al, 1971;Dunn et al, 1978;. For many years the nature of the regulatory mechanisms responsible for coupling of the initiation of sporulation with cell cycle progression remained unclear.…”

Section: Asymmetry and The Determination Of Cell Fatementioning

confidence: 99%

From spores to antibiotics via the cell cycle

Errington

2010

Microbiology

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Spore formation in Bacillus subtilis is a superb experimental system with which to study some of the most fundamental problems of cellular development and differentiation. Work begun in the 1980s and ongoing today has led to an impressive understanding of the temporal and spatial regulation of sporulation, and the functions of many of the several hundred genes involved. Early in sporulation the cells divide in an unusual asymmetrical manner, to produce a small prespore cell and a much larger mother cell. Aside from developmental biology, this modified division has turned out to be a powerful system for investigation of cell cycle mechanisms, including the components of the division machine, how the machine is correctly positioned in the cell, and how division is coordinated with replication and segregation of the chromosome. Insights into these fundamental mechanisms have provided opportunities for the discovery and development of novel antibiotics. This review summarizes how the bacterial cell cycle field has developed over the last 20 or so years, focusing on opportunities emerging from the B. subtilis system.

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The Relationship Between DNA Replication and the Induction of Sporulation in Bacillus subtilis

Cited by 38 publications

References 22 publications

Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis

Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis

Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor.

From spores to antibiotics via the cell cycle

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