Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis

Cabeen, Matthew T.; Jacobs‐Wagner, Christine

doi:10.1083/jcb.200708001

Cited by 73 publications

(67 citation statements)

References 67 publications

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“…PBP localization studies performed in bacilli and cocci suggest that recruitment of these proteins is mediated by structural determinants of the cytoskeleton (e.g. the FtsZ ring at the septum and actin-like filaments along the longitudinal axis of the cell) (3,8,9). Substrate availability also appears to be important for proper localization and activity of PBPs, as was reported for Escherichia coli (10) and more recently for Streptococcus pneumoniae (11) and Staphylococcus aureus (12).…”

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confidence: 84%

Functional and Morphological Adaptation to Peptidoglycan Precursor Alteration in Lactococcus lactis

Deghorain

Fontaine

David

et al. 2010

Journal of Biological Chemistry

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Cell wall peptidoglycan assembly is a tightly regulated process requiring the combined action of multienzyme complexes. In this study we provide direct evidence showing that substrate transformations occurring at the different stages of this process play a crucial role in the spatial and temporal coordination of the cell wall synthesis machinery. Peptidoglycan substrate alteration was investigated in the Gram-positive bacterium Lactococcus lactis by substituting the peptidoglycan precursor biosynthesis genes of this bacterium for those of the vancomycin-resistant bacterium Lactobacillus plantarum. A set of L. lactis mutant strains in which the normal D-Ala-ended precursors were partially or totally replaced by D-Lac-ended precursors was generated. Incorporation of the altered precursor into the cell wall induced morphological changes arising from a defect in cell elongation and cell separation. Structural analysis of the muropeptides confirmed that the activity of multiple enzymes involved in peptidoglycan synthesis was altered. Optimization of this altered pathway was necessary to increase the level of vancomycin resistance conferred by the utilization of D-Lac-ended peptidoglycan precursors in the mutant strains. The implications of these findings on the control of bacterial cell morphogenesis and the mechanisms of vancomycin resistance are discussed.Peptidoglycan (or murein) is a major stress-bearing component of the bacterial cell wall. This polymer is made of glycan chains interconnected by covalent cross-links between short peptides. It acts as an exoskeleton and plays a key role in determining and maintaining cell shape throughout the cell cycle.

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confidence: 84%

Functional and Morphological Adaptation to Peptidoglycan Precursor Alteration in Lactococcus lactis

Deghorain

Fontaine

David

et al. 2010

Journal of Biological Chemistry

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“…Additionally, several bacterial proteins form helical filaments that facilitate their dynamic cellular localization (7,(23)(24)(25)(26). Here, we demonstrated that this abundant structure also directs the nucleoid morphology and may allow the replicated sequences to relocate from one cellular position to another.…”

Section: Discussionmentioning

confidence: 99%

Spatial organization of a replicating bacterial chromosome

Berlatzky

Rouvinski

Ben-Yehuda

2008

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

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Emerging evidence indicates that the global organization of the bacterial chromosome is defined by its physical map. This architectural understanding has been gained mainly by observing the localization and dynamics of specific chromosomal loci. However, the spatial and temporal organization of the entire mass of newly synthesized DNA remains elusive. To visualize replicated DNA within living cells, we developed an experimental system in the bacterium Bacillus subtilis whereby fluorescently labeled nucleotides are incorporated into the chromosome as it is being replicated. Here, we present the first visualization of replication morphologies exhibited by the bacterial chromosome. At the start of replication, newly synthesized DNA is translocated via a helical structure from midcell toward the poles, where it accumulates. Next, additionally synthesized DNA forms a second, visually distinct helix that interweaves with the original one. In the final stage of replication, the space between the two helices is filled up with the very last synthesized DNA. This striking geometry provides insight into the three-dimensional conformation of the replicating chromosome.Bacillus subtilis ͉ bacterial cell biology ͉ DNA replication ͉ nucleoid ͉ replisome F aithful DNA replication and segregation are essential for all prokaryotic and eukaryotic cells to maintain their genomic integrity. The topological features of DNA, combined with its enormous length, raise the fundamental questions of how replication is organized spatially and what is the geometry of the replicating chromosome. These questions are even more crucial for bacteria, because they are capable of initiating a new round of DNA replication before the previous round has been completed, resulting in multifork replication (1). Moreover, bacteria lack a nucleus compartmentalizing their DNA; instead the bacterial DNA mass (nucleoid) occupies the majority of the cytoplasmic space. Nevertheless, the nucleoid appears as a well organized structure in which chromosome replication and partitioning are carried out with remarkable spatial and temporal regulation (2-9).Like many bacteria, Bacillus subtilis has a single circular chromosome (Ϸ4,200 kilobase pairs), where DNA replication is initiated from a single origin (oriC) and proceeds bidirectionally. Visualization of specific B. subtilis chromosomal loci has revealed that, in general, the oriC regions are duplicated at the cell center and then move toward opposite poles, whereas the unduplicated terminus region remains centrally located throughout the replication process (10-14). The replication machinery (replisome) is composed of two complexes, one for each replication fork, that tend to remain at midcell during chromosome duplication (15,16). It has been proposed that unduplicated DNA is pulled into the replisome and newly synthesized DNA is extruded bidirectionally from the complex (4, 16).The spatial and temporal organization of the replicating bacterial chromosome has been elucidated mainly by observing the localization a...

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“…In E. coli, C. crescentus, and B. subtilis, MreC localizes helically along the cylindrical walls of cells (15,31,67). In E. coli and B. subtilis, the helical sidewall localization of MreC is organized by MreB family proteins (4,25,26,58,66), whereas the migration of MreC to the paraseptal rings adjacent to the FtsZ ring of dividing E. coli cells is independent of MreB or MreD (67). In contrast to E. coli and B. subtilis, the helical filament formation of MreC is independent of MreB in C. crescentus, where MreC is located detached from the inner membrane in the periplasm (15).…”

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confidence: 99%

“…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).…”

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confidence: 99%

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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Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis

Cited by 73 publications

References 67 publications

Functional and Morphological Adaptation to Peptidoglycan Precursor Alteration in Lactococcus lactis

Functional and Morphological Adaptation to Peptidoglycan Precursor Alteration in Lactococcus lactis

Spatial organization of a replicating bacterial chromosome

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

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