Chapter 9 : Cell Division during Growth and Sporulation

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Rapid progress has recently been made in understanding the division process in . One factor in this has been the genome sequencing project, which allowed identification of the remaining homologues in of division genes first characterized in . The second factor has been the development of powerful cytological methods based on fluorescence microscopy, partly originating in the need to observe cell-specific events occurring during sporulation. The application of immunofluorescence microscopy and utilization of fusions has enabled the subcellular localization of division proteins to be determined. Most studies of the regulation of cell division have focused on the effects of growth rate on division frequency and on the coordination of division with chromosome replication. Spores contain single, completely replicated chromosomes, and, under appropriate conditions, a population of spores can be induced to outgrow and progress through one or more cell cycles in a relatively synchronous manner. Studies with conditional cell division mutants have shown that all of the genes needed for division in vegetative growth that have been tested are also required for sporulation, with the possible exception of . It is notable that the FtsZ and SpoIIE bands at the two poles of the predivisional cells often differ in intensity, suggesting that they are nonequivalent. There is now overwhelming evidence that the earliest detectable event at the impending division site is the assembly of a ring of FtsZ protein.

Citation: Errington J, Daniel R. 2002. Cell Division during Growth and Sporulation, p 97-109. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch9

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Integral Membrane Proteins
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Image of FIGURE 1

Cell division during growth and sporulation of The left side of the figure shows a schematic of the vegetative cycle; the sporulation cycle, induced by starvation, is on the right. Gray shading shows the cell wall layers composed of peptidoglycan and teichoic acids outside the cell membrane, which is represented by the thin black line. Medial division occurs by invagination of membrane and cell wall layers to produce a septum, and division is completed by cell separation. The daughter cells then continue growing until they more or less double in length, at which point division occurs again. Following starvation, the cells switch to sporulation, during which the position of the division septum is switched to a subpolar position. Morphologically, the septum is also much thinner, with less wall material and probably no teichoic acids (see text). Several hours later, spore development is finished. The mother cell lyses to release the mature spore, and the cycle is completed by germination and outgrowth to regenerate the vegetative cell.

Citation: Errington J, Daniel R. 2002. Cell Division during Growth and Sporulation, p 97-109. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch9
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Image of FIGURE 2

Hierarchy of assembly of division proteins. Summary of the results of experiments examining targeting of division proteins to the predivisional ring and their dependence on other division proteins. Results obtained for FtsW and FtsA are tentative, as indicated by the question marks. Earlier assembling proteins are shown to the left

Citation: Errington J, Daniel R. 2002. Cell Division during Growth and Sporulation, p 97-109. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch9
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Image of FIGURE 3

Model for division site selection by the Min-DivIVA system. Various steps in a cell cycle are shown, beginning with a newborn cell (A). The oval shaded structure represents the nucleoid, which segregates into two separate nucleoids following the completion of a round of DNA replication (B). White triangles represent DivIVA protein, and the dark gray stripes represent MinD (probably associated with the MinC division inhibitor). The small open circles represent FtsZ monomers. These tend to be excluded from the vicinity of the nucleoid. Nucleation of FtsZ to produce the Z ring begins in the DNA-free zone between the nucleoids (C). The filled black circles (D) indicate that the division apparatus has matured beyond the point at which its formation can be prevented by MinCD, possibly by recruitment of other division proteins that stabilize the Z ring. This maturation of the Z ring allows recruitment of DivIVA to midcell (E), which in turn allows targeting of MinD (F). Following cell division (G), both new cell poles have active MinD, preventing further polar (minicell) divisions from taking place. Reproduced with permission from reference 79.

Citation: Errington J, Daniel R. 2002. Cell Division during Growth and Sporulation, p 97-109. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch9
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Image of FIGURE 4

Reorganization of the cell division cycle during sporulation and its regulation. The central part of the figure shows several steps in the switch from medial to polar division after the initiation of sporulation. Thin dotted lines show immature predivisional rings containing FtsZ protein and probably SpoIIE. Thick dotted lines show mature division machinery with the other division proteins, through to PBP 2B, just prior to division. The first cell (left) is just reaching the crucial size at which it would commit to central division when the starvation stimulus is sensed. Under vegetative conditions, or in the absence of a functional gene, the cell would assemble the division machinery and divide at midcell, as shown below. In the wild type, the midcell site is not used, for reasons that are not yet understood, and the division machinery instead assembles close to the cell poles. Although both poles can be used, development of the division apparatus is usually more advanced at one pole (upper in this case) than at the other. In mutants, both poles are targeted, but neither predivisional Z ring matures to the point where division can occur. In the wild type, sep-tation now occurs at one pole, and development of the Z ring at the second pole continues until it is blocked by one or more genes expressed in the mother cell as a result of the signal transduction cascade leading to activation of σ. This leads to disassembly and/or degradation of the various division proteins in the mother cell compartment. In the absence of any component of the signal transduction cascade, e.g., in or mutants, the second Z ring goes on to mature, and a second polar septum is formed, generating two presporelike cells.

Citation: Errington J, Daniel R. 2002. Cell Division during Growth and Sporulation, p 97-109. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch9
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104. Scheffers, D.-J.,, T. den Blaauwen,, and A. J. M. Driessen. 2000. Non-hydrolysable GTP-γ -S stabilizes the FtsZ polymer in a GDP-bound state. Mol. Microbiol. 35: 12111219.
105. Shapiro, L.,, and R. Losick. 1997. Protein localization and cell fate in bacteria. Science 276:712718.
106. Sharpe, M. E.,, P. M. Hauser,, R. G. Sharpe,, and J. Errington. 1998. Bacillus subtilis cell cycle as studied by fluorescence microscopy: constancy of the cell length at initiation of DNA replication and evidence for active nucleoid partitioning. J. Bacteriol. 180:547555.
107. Sievers, J.,, and J. Errington. 2000. The Bacillus subtilis cell division protein FtsL localizes to sites of septation and interacts with DivIC. Mol. Microbiol. 34:846855.
108. Sievers, J.,, and J. Errington. Unpublished results.
109. Smith, T. j.,, S. A. Blackman,, and S. J. Foster. 2000. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249262.
110. Stragier, P.,, and R. Losick. 1996. Molecular genetics of sporulation in Bacillus subtilis. Annu. Rev. Genet. 30:297341.
111. Thomaides, H. B.,, M. Freeman,, M. El Karoui,, and J. Errington. Division-site-selection protein DivIVA of Bacillus subtilis has a second distinct function in chromosome segregation during sporulation. Genes Dev., in press.
112. Van Alstyne, D.,, and M. I. Simon. 1971. Division mutants of Bacillus subtilis: isolation and PBS1 transduction of division-specific markers. J. Bacteriol. 108:13661379.
113. Varley, A. W.,, and G. C. Stewart. 1992. The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (MinCD) and cell shape (MreBCD) determinants. J. Bacteriol. 174:67296742.
114. Wang, L.,, M. K. Khattar,, W. D. Donachie,, and J. Lutkenhaus. 1998. Ftsl and FtsW are localized to the septum in Escherichia coli. J. Bacteriol. 180:28102816.
115. Wang, X.,, J. Huang,, A. Mukherjee,, C. Cao,, and J. Lutkenhaus. 1997. Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J. Bacteriol. 179:55515559.
116. Wang, X.,, and J. Lutkenhaus. 1993. The FtsZ protein of Bacillus subtilis is localized at the division site and has GT-Pase activity that is dependent upon FtsZ concentration. Mol. Microbiol. 9:435442.
117. Woldringh, C. L.,, and N. Nanninga,. 1985. Structure of the nucleoid and cytoplasm in the intact cell, p. 161197. In N. Naninga (éd.), Molecular Cytology of Escherichia coli. Academic Press, London, England.
118. Wu, L. J.,, R. A. Daniel,, H. Scowcroft,, and J. Errington. Unpublished results.>
119. Wu, L. J.,, A. Feucht,, and J. Errington. 1998. Prespore-specific gene expression in Bacillus subtilis is driven by sequestration of SpoIIE phosphatase to the prespore side of the asymmetric septum. Genes Dev. 12:13711380.
120. Wu, L. J.,, A. H. Franks,, and R. G. Wake. 1995. Replication through the terminus region of the Bacillus subtilis chromosome is not essential for the formation of a division septum that partitions the DNA. J. Bacteriol. 177: 57115715.
121. Wu, L. J.,, P. J. Lewis,, R. Allmansberger,, P. M. Hauser,, and J. Errington. 1995. A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis. Genes Dev. 9:13161326.
122. Yanouri, A.,, R. A. Daniel,, J. Errington, and C. E. Buchanan. 1993. Cloning and sequencing of the cell division gene pbpB, which encodes penicillin-binding protein 2B in Bacillus subtilis. J. Bacteriol. 175:76047616.


Generic image for table

Cell division

Position in kilobase pairs based on data in the SubtiList database ( ) (http://genolist.pasteur.fr/SubtiList). Where the gene has not been identified, an estimated position is given, with the published genetic map location in parentheses.

Citation: Errington J, Daniel R. 2002. Cell Division during Growth and Sporulation, p 97-109. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch9

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