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Themes and Variations in Prokaryotic Cell Division FEMS Microbiology Reviews 24 (2000) 531^548 www.fems-microbiology.org Themes and variations in prokaryotic cell division William Margolin * Department of Microbiology and Molecular Genetics, University of Texas-Houston Medical School, 6431 Fannin, Houston, Texas 77030, USA Received 26 January 2000; received in revised form 6 June 2000; accepted 20 June 2000 Downloaded from https://academic.oup.com/femsre/article/24/4/531/510989 by guest on 04 October 2021 Abstract Perhaps the biggest single task facing a bacterial cell is to divide into daughter cells that contain the normal complement of chromosomes. Recent technical and conceptual breakthroughs in bacterial cell biology, combined with the flood of genome sequence information and the excellent genetic tools in several model systems, have shed new light on the mechanism of prokaryotic cell division. There is good evidence that in most species, a molecular machine, organized by the tubulin-like FtsZ protein, assembles at the site of division and orchestrates the splitting of the cell. The determinants that target the machine to the right place at the right time are beginning to be understood in the model systems, but it is still a mystery how the machine actually generates the constrictive force necessary for cytokinesis. Moreover, although some cell division determinants such as FtsZ are present in a broad spectrum of prokaryotic species, the lack of FtsZ in some species and different profiles of cell division proteins in different families suggests that there are diverse mechanisms for regulating cell division. ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. Keywords: Bacterium; Cell division; Septation; Binary ¢ssion Contents 1. Introduction .......................................................... 532 2. Cell division: a major developmental event . .................................. 532 3. FtsZ, the keystone of the cell division apparatus . ............................ 532 4. FtsA and Z-interacting protein A (ZipA), FtsZ-interacting proteins ................. 533 5. FtsK and FtsW, polytopic integral membrane proteins ........................... 536 6. The bitopic cell division proteins ........................................... 536 7. A conserved septum/cell wall synthesis cluster ................................. 537 8. Other genes and factors that a¡ect cell division ................................ 537 9. Cell division in other model systems: B. subtilis ................................ 537 10. Cell division in other model systems: C. crescentus ............................. 538 11. Cocci ............................................................... 538 12. Chlamydia ........................................................... 539 13. Mycoplasma and L-forms ................................................ 539 14. Archaea . ........................................................... 539 15. Organelles . ........................................................... 540 16. Factors involved in the speci¢cation of the division plane . ....................... 540 16.1. The Min system . ................................................. 540 16.2. The nucleoid ...................................................... 542 16.3. A new model for E. coli division site placement ............................ 543 17. Perspectives ........................................................... 543 Acknowledgements . ...................................................... 544 References ............................................................... 544 * Tel.: +1 (713) 500-5452; Fax: +1 (713) 500-5499; E-mail: [email protected] 0168-6445 / 00 / $20.00 ß 2000 Federation of European Microbiological Societies. Published by Elsevier Science B.V. All rights reserved. PII: S0168-6445(00)00038-3 FEMSRE 690 29-8-00 Cyaan Magenta Geel Zwart 532 W. Margolin / FEMS Microbiology Reviews 24 (2000) 531^548 1. Introduction been fully sequenced: Aeropyrum pernix, a crenarchaeon, and Ureaplasma urealyticum, a mycoplasma species. De- In order to proliferate vegetatively, all cells ¢rst dupli- spite these and probably other exceptions, FtsZ is present cate their chromosomes into separate subcellular compart- in lower and higher plants and appears to be important ments, then split by dividing their cytoplasms somewhere for chloroplast division (see Section 15). between the chromosomes to yield progeny cells. This ba- In E. coli, FtsZ appears to act at the earliest known step sic process of cell division is conceptually similar in eu- in cell division. Conditional mutants of ftsZ in E. coli fail karyotic and prokaryotic cells. There are several advan- to divide, yielding long ¢lamentous cells that replicate and tages of studying cell division in prokaryotes: the process segregate their chromosomes but have no sign of any di- is likely to be simpler, there are several outstanding model vision septa or cellular constrictions (thus the term `fts', systems for study such as Escherichia coli, Caulobacter for `¢lamentous temperature sensitive'). FtsZ is also the crescentus and Bacillus subtilis, and a greater understand- target of SulA protein, synthesis of which is induced ing of cell division in bacteria may lead to novel therapeu- upon DNA damage [10]. SulA transiently prevents FtsZ tic antimicrobial compounds. Over the last decade, advan- from functioning in cell division, thus inhibiting unwanted Downloaded from https://academic.oup.com/femsre/article/24/4/531/510989 by guest on 04 October 2021 ces in cytological and genomic technologies have greatly cell divisions until the damage to the chromosome can be increased our understanding of cell division in prokary- repaired [11^13]. otes, particularly in the model systems. It is likely, how- A structural role for FtsZ was initially suggested by its ever, that we will ¢nd a diversity of cell division mecha- abundance, about 15 000 monomers per average E. coli nisms that mirror the diversity of microbial life. The cell [14], and by its localization by immunogold labeling purpose of this review is to summarize the common to a ring structure at the future site of division [15]. Lo- themes of cell division as well as the likely variations cated at the cytoplasmic membrane, the Z ring, as it is among the vast prokaryotic world. called, appears to contract dynamically along with the membrane as it invaginates during formation of the divi- sion septum. The Z ring has also been detected by light 2. Cell division: a major developmental event microscopy in whole E. coli cells and in other bacteria and archaea by using either immuno£uorescence or green £uo- In many rod-shaped bacteria such as E. coli and B. rescent protein (GFP) fusions to FtsZ [16^20]. These subtilis, cell division involves the synthesis of a septum, methods con¢rmed the previous ¢ndings, demonstrated with some constriction also occurring in addition to sep- that Z rings occur in diverse prokaryotic species, and the tation in E. coli [1]. In others, such as C. crescentus, cell GFP studies directly demonstrated the dynamic properties division appears to occur exclusively by simultaneous con- of the Z ring during cell growth and division of E. coli striction of the entire cell envelope, resulting in tapered [21]. poles [2]. In these cases and in others, including cocci The localization of FtsZ to a ring structure at the divi- and in species such as cyanobacteria that form chains of sion site of E. coli (Figs. 1A and 2A) suggests that FtsZ cells, it is clear that cell division is a major developmental protein forms some type of cytoskeletal structure [5]. Un- event, arguably the predominant cellular event in the veg- fortunately, an actual FtsZ structure has not yet been vi- etative life cycle of a bacterial cell [3]. To redirect cell wall sualized in thin sections of E. coli cells. However, much growth in a new direction (formation of the septum) and/ has been learned about the properties of FtsZ protein that or to provide the constrictive force at a single location in can help formulate a model about its structural role in cell the cell, particularly against several atmospheres of turgor division. There is now overwhelming evidence in favor of pressure, it is easy to imagine that a fairly complex mo- the idea that FtsZ is a homolog of tubulin, the ubiquitous lecular machine must be required. Recent evidence indi- eukaryotic cytoskeletal protein involved in many essential cates that a protein machine dedicated to the process of cellular processes including mitosis [7]. Despite only lim- cell division is assembled between segregated chromo- ited primary sequence homology centered around a GTP somes at the proper time [4^6]. The key to this machine's binding motif termed the `tubulin signature sequence' [22^ assembly is FtsZ [7^9]. 25], the recently solved crystal structures of FtsZ and tu- bulin show extensive structural homology throughout the proteins [26]. In addition, FtsZ, like tubulin, binds and 3. FtsZ, the keystone of the cell division apparatus hydrolyzes GTP and assembles into proto¢laments that have structures similar to those within microtubules FtsZ is by far the most highly conserved of the known [27,28]. This assembly is GTP-dependent [29,30] and dis- cell division proteins. It is present in most species of pro- assembly occurs when the GTP is exhausted, suggesting karyotes examined to date (Table 1). Interestingly, it is not that FtsZ polymers, like microtubules, are dynamically present in the obligately intracellular
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