Bacterial Shape: Two-Dimensional Questions and Possibilities

Young, Kevin

doi:10.1146/annurev.micro.112408.134102

Cited by 138 publications

(149 citation statements)

References 113 publications

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“…Two-state model of PG biosynthesis in ovococcus bacteria, such as S. pneumoniae. To attain an ellipsoid shape, two machineries have been proposed that carry out peripheral and septal PG synthesis (12,71,72). At the start of a division cycle, components of both machines locate to the equators of cells (bottom).…”

Section: Methodsmentioning

confidence: 99%

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The Requirement for Pneumococcal MreC and MreD Is Relieved by Inactivation of the Gene Encoding PBP1a

2011

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Three basic patterns of peptidoglycan (PG) synthesis have emerged from the study of rod-shaped (bacillus), spherical (coccus), and ellipsoid (ovococcus) bacteria (reviewed in references 12, 71, and 72). In rod-shaped bacteria, like Escherichia coli, Bacillus subtilis, and Caulobacter crescentus, PG synthesis occurs at two locations catalyzed by distinct sets of proteins (12,35,36,71). Lateral PG synthesis elongates the side walls of these bacteria and results in their rod shape (12,35,71). Lateral PG synthesis is mediated by actin-like MreB paralogue proteins, which form filamentous helical structures in spirals over the length of cells (12,35,66). MreB is thought to organize the MreC and MreD proteins, which in turn recruit specific penicillin-binding proteins (PBPs) and other division proteins that catalyze lateral PG formation (26,54,55,70). Septal PG synthesis is organized by FtsZ ring formation, followed by the orderly assembly of the divisome complex, which includes a set of PBPs different from those involved in lateral PG synthesis (16,22,23). The mutational interruption of lateral or septal PG synthesis of rod-shaped bacteria generally results in the formation of spherical or elongated cells, respectively (3, 4, 9, 31). Although useful, this two-state model is obviously an oversimplification (35), and recent results reveal that MreB, MreC, MreD, and specific PBPs also form annular rings adjacent to FtsZ rings at the septa of dividing E. coli cells (67). Moreover, some PBPs and division regulators, such as PBP1 and GpsB of B. subtilis, shuttle between the lateral and septal PG synthesis machineries (9).Much less is known about the mechanisms of PG synthesis in coccus and ovococcus species. In spherical species, such as Staphylococcus aureus, only a septal PG synthesis machinery seems to be present (20,47,72), although S. aureus still encodes homologues of proteins like MreC and MreD that mediate lateral PG synthesis in rod-shaped bacteria (35). In contrast, ovococcus species, such as Streptococcus pneumoniae and Lactococcus lactis, form American football-shaped cells by a combination of peripheral sidewall and septal PG synthesis that occurs in the midcell regions of dividing cells (Fig. 1) (11,42). Ovococcus species lack an MreB homologue, and peripheral and septal PG synthesis are likely coordinated with and organized by FtsZ ring formation (64,65,72). Because two modes of PG biosynthesis are required to form ellipsoidshaped bacteria, models have been proposed for two different PG synthesis machineries (18,21,33,72). Based on the composition of the complexes in rod-shaped cells, it has been hypothesized that specific sets of homologous cell division proteins mediate peripheral (MreC, MreD, RodA, and PBP2b) and septal (FtsZ, EzrA, PBP2x, FtsW, and DivIB/FtsL/DivIC) PG synthesis in ovococcus bacteria (72). A recent study correlating the effects of mutations or antibiotic treatments to changes in cell shapes supports the idea that the PBP2x and PBP2b class B transpeptidases are associated with septal and p...

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Section: Methodsmentioning

confidence: 99%

“…In rod-shaped bacteria, like Escherichia coli, Bacillus subtilis, and Caulobacter crescentus, PG synthesis occurs at two locations catalyzed by distinct sets of proteins (12,35,36,71). Lateral PG synthesis elongates the side walls of these bacteria and results in their rod shape (12,35,71).…”

mentioning

confidence: 99%

The Requirement for Pneumococcal MreC and MreD Is Relieved by Inactivation of the Gene Encoding PBP1a

2011

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“…This gene encodes an MreB homologue, a structural protein that forms filaments that spiral around the periphery of the cell (Jones et al, 2001). MreB interacts with membrane proteins and peptidoglycan synthases in a complex that directs cell wall growth (Young, 2010). A lower abundance of MreB also points to diminished cell wall-building activity.…”

Section: Cell Envelope-related Functionsmentioning

confidence: 99%

Proteomic and transcriptomic analysis of the response to bile stress of Lactobacillus casei BL23

Alcántara

Zúñiga

2012

Microbiology

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Lactobacillus casei is a lactic acid bacterium commonly found in the gastrointestinal tract of animals, and some strains are used as probiotics. The ability of probiotic strains to survive the passage through the gastrointestinal tract is considered a key factor for their probiotic action. Therefore, tolerance to bile salts is a desirable feature for probiotic strains. In this study we have characterized the response of L. casei BL23 to bile by a transcriptomic and proteomic approach. The analysis revealed that exposure to bile induced changes in the abundance of 52 proteins and the transcript levels of 67 genes. The observed changes affected genes and proteins involved in the stress response, fatty acid and cell wall biosynthesis, metabolism of carbohydrates, transport of peptides, coenzyme levels, membrane H + -ATPase, and a number of uncharacterized genes and proteins. These data provide new insights into the mechanisms that enable L. casei BL23 to cope with bile stress.

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“…Previous studies have characterized selective pressures favoring particular shapes (7,(9)(10)(11): for example, highly viscous environments may select for the helical cell morphologies observed in spirochete bacteria (12). Thus far, these studies have predominantly focused on selective pressures acting at the level of the individual cell.…”

mentioning

confidence: 99%

Cell morphology drives spatial patterning in microbial communities

Smith

Davit

Osborne

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

156

138

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The clearest phenotypic characteristic of microbial cells is their shape, but we do not understand how cell shape affects the dense communities, known as biofilms, where many microbes live. Here, we use individual-based modeling to systematically vary cell shape and study its impact in simulated communities. We compete cells with different cell morphologies under a range of conditions and ask how shape affects the patterning and evolutionary fitness of cells within a community. Our models predict that cell shape will strongly influence the fate of a cell lineage: we describe a mechanism through which coccal (round) cells rise to the upper surface of a community, leading to a strong spatial structuring that can be critical for fitness. We test our predictions experimentally using strains of Escherichia coli that grow at a similar rate but differ in cell shape due to single amino acid changes in the actin homolog MreB. As predicted by our model, cell types strongly sort by shape, with round cells at the top of the colony and rod cells dominating the basal surface and edges. Our work suggests that cell morphology has a strong impact within microbial communities and may offer new ways to engineer the structure of synthetic communities.biofilms | cell morphology | biophysics | self-organization | synthetic biology S ingle-celled microorganisms such as bacteria display significant morphological diversity, ranging from the simple to the complex and exotic (1-3). Phylogenetic studies indicate that particular morphologies have evolved independently multiple times, suggesting that the myriad shapes of modern bacteria may be adaptations to particular environments (4-6). Microbes can also actively change their morphology in response to environmental stimuli, such as changes to nutrient levels or predation (7,8). However, understanding when and why particular cell shapes offer a competitive edge remains an unresolved question in microbiology.Previous studies have characterized selective pressures favoring particular shapes (7, 9-11): for example, highly viscous environments may select for the helical cell morphologies observed in spirochete bacteria (12). Thus far, these studies have predominantly focused on selective pressures acting at the level of the individual cell. However, many species live in dense, surfaceassociated communities known as biofilms, which are fundamental to the biology of microbes and how they affect us-playing major roles in the human microbiome, chronic diseases, antibiotic resistance, biofouling, and waste-water treatment (13-17). As a result, there has been an intensive effort in recent years to understand how the biofilm mode of growth affects microbes and their evolution (18, 19), but we know very little of the importance of cell shape for biofilm biology.In biofilms, microbial cells are often in close physical contact, making mechanical interactions between neighboring cells particularly significant. Recent studies have suggested that rodshaped cells can drive collective behaviors in microbial g...

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Bacterial Shape: Two-Dimensional Questions and Possibilities

Cited by 138 publications

References 113 publications

The Requirement for Pneumococcal MreC and MreD Is Relieved by Inactivation of the Gene Encoding PBP1a

The Requirement for Pneumococcal MreC and MreD Is Relieved by Inactivation of the Gene Encoding PBP1a

Proteomic and transcriptomic analysis of the response to bile stress of Lactobacillus casei BL23

Cell morphology drives spatial patterning in microbial communities

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