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Sculpting the Bacterial Cell Review CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Current Biology 19, R812–R822, September 15, 2009 ª2009 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2009.06.033 Sculpting the Bacterial Cell Review William Margolin tuberculosis is a pleomorphic rod that often branches or swells at the poles; Staphylococcus aureus is a sphere, Prokaryotes come in a wide variety of shapes, determined and Streptococcus pneumoniae is ovoid, with pointed polar largely by natural selection, physical constraints, and caps. Then there are even more interesting ones, including patterns of cell growth and division. Because of their Streptomyces, which form fungi-like mycelial mats and aerial relative simplicity, bacterial cells are excellent models for hyphae; Caulobacter crescentus, which forms a curved rod how genes and proteins can directly determine mor- like V. cholerae but with tapered ends and a polar stalk at phology. Recent advances in cytological methods for one end. Archaea also have diverse shapes. While they bacteria have shown that distinct cytoskeletal filaments generally have similar shapes and sizes as bacteria, either composed of actin and tubulin homologs are important round or rod-like, one extreme thermophile (Haloquadratum for guiding growth patterns of the cell wall in bacteria, walsbyi) forms flat squares. Some bacteria are tiny rods, and that the glycan strands that constitute the wall are such as Bdellovibrio bacteriovorus, which hunts and invades generally perpendicular to the direction of growth. This other bacteria and grows in their cytoplasm. Others are cytoskeleton-directed cell wall patterning is strikingly remi- hundreds of microns long and over 20 microns wide, such niscent of how plant cell wall growth is regulated by micro- as Epulopiscium fishelsoni. All this diversity does not even tubules. In rod-shaped bacilli, helical cables of actin-like take into account the multicellular structures that many MreB protein stretch along the cell length and orchestrate bacteria can form, such as the long chains of Anabaena or elongation of the cell wall, whereas the tubulin-like FtsZ the flower-shaped fruiting bodies of Stigmatella aurantiaca. protein directs formation of the division septum and the re- Even bacteria without walls, such as the mycoplasmas, sulting cell poles. The overlap and interplay between these have their own distinctive shapes organized by an internal two systems and the peptidoglycan-synthesizing enzymes cytoskeletal scaffold. More detailed information about these they recruit are the major driving forces of cylindrical species and their shapes can be found in a recent compre- shapes. Round cocci, on the other hand, have lost their hensive review [5]. MreB cables and instead must grow mainly via their division Why have such morphological diversity? The answer is septum, giving them their characteristic round or ovoid partly because of selective pressures and in part from phys- shapes. Other bacteria that lack MreB homologs or even ical constraints [6]. One important selective pressure is com- cell walls use distinct cytoskeletal systems to maintain their petition for nutrients, which can be optimized by increasing distinct shapes. Here I review what is known about the the surface area relative to total cell volume. The C. cres- mechanisms that determine the shape of prokaryotic cells. centus stalk is an extreme example of increasing surface area for nutrient foraging in nutrient-poor environments [7]. Introduction Other selective pressures on shape include motility and The control of cell shape is ultimately an epigenetic process, resistance to predation [8]. with molecules exerting their effects on various physical One key physical constraint is diffusion limitation. Without constraints. Bacteria like Escherichia coli offer an excellent obvious cytoplasmic transport mechanisms, the scope of opportunity to understand shape determination at the cell sizes for most bacteria is quite narrow, sufficiently small molecular level. The cells are relatively simple, the genomes to accommodate diffusion-limited processes but large and proteomes manageable in size, and there are many enough to house the necessary macromolecules, such as mutants in a single gene that give rise to altered shape. ribosomes and chromosomal DNA, to maintain and dupli- Like plant cells, most bacteria have walls, and the shape of cate the cell. Another physical constraint is turgor pressure. their cells is largely governed by how the wall grows. For Because of relatively low water activity in the cytoplasm rela- most bacteria, then, understanding how the wall grows will tive to the outside environment, bacteria are essentially pres- be crucial for obtaining a complete picture of cell shape sure vessels, and the cell wall must be oriented to provide determination. Because the cell wall or murein (also called sufficient strength to counteract turgor forces of several the sacculus) is one large macromolecule, both the building hundred kilopascals in Gram-negative bacteria and as high and the turnover of this large structure help to determine cell as 3 megapascals in Gram-positive bacteria [9,10]. This pla- shape. A number of recent reviews cover the biochemistry ces limitations on the varieties of shapes bacterial cells can and cell biology of bacterial murein in detail [1–4]. have. However, there are examples where turgor pressure is probably low, such as in extreme halophiles where the A Great Diversity of Shapes molar levels of salt inside the cell are similar to those outside Despite usually being constrained by a cell wall, the shapes [11]. This, along with a putative internal cytoskeleton, might of bacteria are highly diverse, reflecting their large phyloge- explain why some species of halophilic archaea can assume netic range. For example, of the relatively straightforward triangular and square shapes with sharp corners that are not shapes, E. coli and Bacillus subtilis are straight rods; Vibrio seen in other species. cholerae is a curved rod; the Borrelia burgdorferi spirochete For a long time, these selective and physical forces were is a flat wave, an elongated and iterated version of the curved thought to be the main determinants of bacterial shape, in rod; Spiroplasma species are helix-shaped; Mycobacterium part because bacteria were not supposed to have cytoskel- etons. The genetic and cytoskeletal determinants of bacte- Department of Microbiology and Molecular Genetics, University of rial cell size and shape have only been appreciated relatively Texas Medical School at Houston, 6431 Fannin Street, Houston, TX recently, largely because of the sequencing of multiple 77030, USA. genomes and fluorescent protein tags for visualizing protein E-mail: [email protected] localization in living cells. Special Issue R813 Figure 1. Basic growth modes of six repre- A sentative species. B. subtilis E. coli C. crescentus Shown are three species that contain MreB (A) and three species that lack MreB (B), with modes of growth summarized below for each. For each species, the arrow refers to the transition between a newborn cell and one at the final stages of division prior to cell separation and new pole formation. For each stage, areas of the cell probably not engaged in significant peptidoglycan synthesis are out- lined in blue; areas actively synthesizing Sidewall, then septum Sidewall, then Sidewall, then peptidoglycan are outlined in other colours. septum + constriction constriction only Areas of MreB-dependent wall growth are shown in red or magenta; the magenta in B S. pneumoniae S. aureus C. glutamicum C. crescentus indicates slower growth rela- tive to the red, because of the inhibitory effects of crescentin. Areas of FtsZ-depen- dent wall growth are shown in green. Solid green outlines indicate septal wall synthesis, and green dots indicate probable locations of active FtsZ-directed sidewall synthesis preceding cell division. Areas of DivIVA- dependent wall growth are shown in orange. In species with septal growth but no constric- tion, proper formation of the new pole Septum + sidewall Septum only Tip growth, then septum requires splitting of the septum and turgor- Current Biology dependent reshaping. For simplicity, there are three main types of bacterial cell the wall, and a number of models have been proposed to shape to consider: cylindrical, typified by E. coli or B. subtilis, explain this type of insertion of new peptidoglycan [2]. but also including curved rods such as C. crescentus; ovococ- Recent cryo-electron tomography and atomic force micros- cal, typified by S. pneumoniae; and coccal, typified by copy data support the model in which individual glycan S. aureus (Figure 1). Cylindrical cells grow mainly by extending strands are coiled together into larger fibers, and once the length of the cylinder, and new cell poles are synthesized inserted into the existing peptidoglycan structure (the during a relatively short time window at cell division. This sacculus) under turgor pressure, stretch to assume an orien- shape has its advantages over a round shape, but requires tation roughly perpendicular to the long axis of the cell [14]. more sophisticated controls. Ovococci and the cocci both In contrast, the peptide bridges connecting glycan strands grow mainly via their division septa, but ovococci undergo are oriented parallel to the long axis. The end result, at least some length extension, whereas cocci grow exclusively via in B. subtilis, is that the glycan strands appear
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