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Alternatives to Binary Fission in Bacteria REVIEWS ALTERNATIVES TO BINARY FISSION IN BACTERIA Esther R. Angert Abstract | Whereas most prokaryotes rely on binary fission for propagation, many species use alternative mechanisms, which include multiple offspring formation and budding, to reproduce. In some bacterial species, these eccentric reproductive strategies are essential for propagation, whereas in others the programmes are used conditionally. Although there are tantalizing images and morphological descriptions of these atypical developmental processes, none of these reproductive structures are characterized at the molecular genetic level. Now, with newly available analytical techniques, model systems to study these alternative reproductive programmes are being developed. NUCLEOID Conceptually, cell propagation by binary fission is a segregates into incipient daughter cells in a controlled The highly organized simple process; a cell merely needs to grow to twice its size, manner2.Although the timing of replication initiation chromosomal DNA of a and then split in two. But to remain competitive, let alone with respect to the cell-division cycle, and the mainte- bacterial cell. viable, a prokaryotic cell must divide at the appropriate nance of NUCLEOID position are tightly controlled in bacte- CYTOSKELETON time and at the correct location in the cell, and must ria, master cell-cycle regulators have only been identified 9,10 Internal network of proteins ensure that each progeny daughter cell receives a com- in C. crescentus .The mechanisms that are responsible that gives a eukaryotic cell its plete complement of genes with high fidelity. Bacterial for the observed rapid movement of replication origins shape, facilitates its movement models that have been used for the study of cell division to polar positions and the segregation of nucleoids have and provides a means of internal include the Gram-negative proteobacterial species yet to be discerned7,11.However, DNA-binding proteins spatial organization. Escherichia coli and Caulobacter crescentus, and the low- that maintain nucleoid structure and that seem to have a GC Gram-positive bacterium Bacillus subtilis.These role in nucleoid segregation (such as SMC in B. subtilis) models have provided insight into cell division and have been identified in various bacteria2,11–13 (TABLE 1). continue to reveal surprising findings1.The cell biology Other cellular components that are implicated in DNA and genetics of cell division in these and other model segregation include the actin-like protein MreB14. organisms have been discussed in recent reviews2–8.As For cell division to occur, the division apparatus important cell-division components are revealed, and must assemble at the site of future cytoplasmic cleav- their genetic homologues in other systems are discovered age. FtsZ,a structural homologue of the eukaryotic and characterized, a framework of core mechanisms that CYTOSKELETAL element tubulin15, assembles into a ring- are conserved among prokaryotes is emerging (TABLE 1). like structure at the centre of the cell16.Other compo- nents of the division machinery assemble at the Binary fission: Bacillus subtilis FtsZ ring. These components redirect cell wall In this review, B. subtilis will be used as a model to intro- growth, and prevent damage to the DNA while the duce the general mechanisms and regulation of cell cell envelope invaginates6,17.Finally, the cell divides to Department of Microbiology, division in bacteria (FIG. 1a).During growth, B. subtilis, in form two approximately equivalent daughter cells. Cornell University, common with other rod-shaped bacteria, elongates. Although many of the genes that are involved in cell 260A Wing Hall, Ithaca, When it reaches about twice its starting length, the cell division have been identified, the mechanisms of New York 14853-5701, USA. e-mail: [email protected] divides in the middle by binary fission. Concurrent with action of these gene products are still under intense doi:10.1038/nrmicro1096 growth, the genetic material of the cell replicates and investigation6,18. 214 | MARCH 2005 | VOLUME 3 www.nature.com/reviews/micro REVIEWS FtsZ is highly conserved among prokaryotes and is Several stabilizing and destabilizing factors ensure that one of the first proteins to assemble at the future cell the Z ring, and therefore the division apparatus, is division site. FtsZ is also the target of cellular mecha- properly positioned. Even among the model systems nisms that regulate the timing of cell division as well there is astonishing variation and flexibility in the as the selection of the cell division site18.In normal, genes and mechanisms that mediate cell division site growing B. subtilis cells, nucleoid occlusion — medi- selection. For example, both E. coli and B. subtilis use ated by the unsegregated nucleoid and associated pro- polar localization of the MinCD complex to prevent teins such as Noc19 — prevents Z-ring assembly at the inappropriate division at the cell poles18.Genetic midcell prior to nucleoid segregation, and the Min sys- analyses have shown that the topological specificity of tem — MinCD and DivIVA — prevents the assembly the MinCD complex is mediated by DivIVA in B. sub- of Z rings near the poles. There is evidence that other tilis and by MinE in E. coli.Although DivIVA and proteins, such as EzrA, affect the stability of FtsZ poly- MinE are functional analogues, they have no signifi- mers to enhance Z-ring assembly only at appropriate cant sequence or structural similarity. In both of these locations. Additional proteins (such as YneA in B. sub- bacteria, MinD interacts with the topological speci- tilis and SulA in E. coli) destabilize Z-ring formation to ficity factor (either DivIVA or MinE) to maintain the prevent cell division when DNA damage is detected20,21. polar localization of MinC,which in turn prevents assembly of the Z ring. In E. coli,MinD travels periodi- 22 Table 1 | Distribution of cell-division proteins among selected bacteria cally from one pole of the cell to the other . One com- plete pole-to-pole oscillation takes place in less than E. coli B. subtilis C. crescentus S. coelicolor one minute. By contrast, the MinD homologue in Nucleoid structural maintenance B. subtilis is pole-associated, but remains static MukB SMC SMC SMC throughout most of the cell cycle23.Despite its role in Nucleoid partitioning enhancing the fidelity of midcell division in many Soj/Spo0J ParA/B ParA/B bacteria, minD is not universally conserved — C. crescentus lacks a recognizable minD homologue8,24. MreB MreB MreB mreB-like* Furthermore, other highly conserved genes that are FtsK SpoIIIE ftsK* ftsK/spoIIIE-like* essential for cell division in E. coli, C. crescentus and Master cell-cycle regulators B. subtilis, most notably ftsZ,are not found in all CtrA prokaryotes25,26.Remarkably, the cell-division machinery GcrA is not as evolutionarily conserved as many of the com- Staking the division site‡ ponents of central metabolism, as outlined in REF.27. This propensity to tolerate modifications of an essential FtsZ FtsZ FtsZ FtsZ process provides opportunities for flexibility to accom- Nucleoid occlusion modate the different ‘lifestyles’ of individual organisms. + Noc w w This review focuses on selected alternative repro- Prevention of polar Z-ring assembly duction modes that are found in the Bacteria, which MinCD MinCD minD-like* include cell-division programmes that result in the MinE formation of multiple offspring, and budding mech- DivIVA (DivIVA)§ anisms. With the advent of microbial genomics and advances in sensitive microscopic techniques Destabilization of extra Z rings (for example, deconvolution microscopy28) and ana- EzrA lytical techniques (for example, mass spectrometric Destabilization of Z rings as part of the SOS response imaging29 and microbeam analyses30), we now have SulA the tools to investigate the mechanisms that underlie DpiA these diverse processes without the need for elaborate YneA genetic analyses in less tractable bacteria. Under- standing the acquisition of these processes in differ- Other division proteins that assemble with the Z ring ent lineages will not only provide insight into the FtsA FtsA FtsA evolution of these reproductive strategies, but will FtsI Pbp2b FtsI ftsI* also shed light on the basic principles of microbial FtsQ DivIB FtsQ FtsQ cell biology that dictate cellular asymmetry, nucleoid FtsL FtsL ftsL* segregation and cell division. It is useful in this con- FtsW FtsW FtsW ftsW* text to consider these mechanisms from an evolu- tionary perspective. In this review, members of only Homologues — proteins that share a common ancestry and have the same function in a cell — are shown in rows that are shaded the same colour, for example, FtsZ. *Potential homologues that have four major bacterial lineages are featured: the low- been identified by sequence comparisons, but that have no assigned function. + indicates a functional GC Gram-positive bacteria, the Cyanobacteria, the mechanism for which no associated genes have been identified. w indicates evidence for a weak phenotype for which no associated gene has been identified. ‡With only a few exceptions, the division Actinobacteria and the Proteobacteria (FIG. 2).A phy- protein FtsZ is conserved among prokaryotes and assembles at the incipient site of cell division in many logenetic perspective is emphasized because model organisms including members of the Archaea, and organelles (such as chloroplasts and mitochondria). systems can serve as a foundation on which to build §DivIVA
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