Taking shape: control of bacterial cell wall biosynthesis
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1 Blackwell Science, LtdOxford, UKMMIMolecular Microbiology XBlackwell Publishing Ltd, 2005? CommentaryBacterial morphogenesg. C. Stewart Molecular Microbiology (2005) 57(5), doi: /j x MicroCommentary Taking shape: control of bacterial cell wall biosynthesis George C. Stewart Department of Veterinary Pathobiology, Life Sciences Center, University of Missouri, Columbia, MO , USA. Summary The characteristic shape of a bacterial cell is a function of the three dimensional architectures of the cell envelope and is determined by the balance between lateral wall extension and synthesis of peptidoglycan at the division septum. The three dimensional patterns of cell wall synthesis in the bacterium Bacillus subtilis is influenced by actin-like proteins that form helical coils in the cell and by the MreCD proteins that link the cytoskeletal elements with the penicillin-binding proteins that carry out peptidoglycan synthesis. Recent genetic studies have provided important clues as to how these proteins are arranged in the cell and how they function to regulate cell shape. Introduction Bacteria exist in characteristic shapes including spheres, cylinders and spirals. Shape is a stable characteristic of a bacterial cell and has historically been used in the definition of a particular species. The characteristic shape of a bacterial cell is determined by the cell envelope. Isolated murein sacculi reflect the specific shape of the cell from which they have been prepared (Höltje, 1998). It follows that the three dimensional assemblies of peptidoglycan precursors into the lateral cell wall of a growing cylindrically shaped bacterium must differ from the incorporation of precursors into the cell wall of spherical or spiral shaped cells. Thus, knowledge of how bacterial shapes are determined is necessary for a complete understanding of cell wall biosynthesis. The ultimate morphology of the cell depends on a complex interplay of many proteins that make up the cell wall biosynthetic apparatus. Certain rod-shaped bacteria can Accepted 6 June, For correspondence. stewartgc@ missouri.edu; Tel. (+1) ; Fax (+1) be converted to spherical shapes, and cocci can elongate into rods, when they are grown in the presence of certain antibiotics or when certain morphogenes are mutated (Lleo et al., 1990). The coccoid bacteria fall into two types, those that can be manipulated to form cylindrical cells and those that cannot. Characterization of the cell morphology mutants has provided considerable insight into the mechanisms of cell wall biosynthesis and cell shape determination. The mrebcd genes The mre (for murein region e ) genes were first identified in Escherichia coli during an analysis of mutants affected in susceptibility to the cell wall synthesis inhibiting antibiotic mecillinam (Wachi et al., 1987; 1989). Mutation of the mreb determinant, or deletion of the mrebcd genes, resulted in the production of cells that maintained a spherical morphology. Analysis of penicillin-binding proteins (PBPs) in these mutants led to the conclusion that MreB protein functions as a negative regulator of PBP 3 (FtsI; Wachi and Matsuhashi, 1989), the enzyme responsible for peptidoglycan synthesis at the division septum (Botta and Park, 1981). PBP 2B performs the same function in Bacillus subtilis (Yanouri et al., 1993; Daniel et al., 2000). Loss of MreB was speculated to increase FtsI activity, leading to hypersepation and a resultant rounding of the cells. These findings were consistent with the two competing sites model for peptidoglycan biosynthesis, which predicts that there are two biosynthetic reactions (referred to as sites) responsible for peptidoglycan biosynthesis and that the two reactions are mutually exclusive (Lleo et al., 1990). A rod-shaped bacterial cell undergoing lateral wall extension as part of the growth process cannot septate. Septal cell wall synthesis occurs at the time of cell division, which prevents lateral wall extension from occurring. Lateral wall extension continues if septal peptidoglycan synthesis is inhibited, leading to cell filamentation, whereas a shift to only septal synthesis causes the formation of coccoid cells. Based on this model, the hyperactivity of FtsI in E. coli would lead to an inhibition of lateral wall extension and thus new cell wall synthesis would only result from the formation of the division septum and would generate cocci Blackwell Publishing Ltd
2 1178 G. C. Stewart Table 1. Examples of mrec-containing species. Gram-negative rods Gram-positive rods Curved rods Spirochetes Cocci Caulobacter crescentus Bacillus anthracis Bdellovibrio bacteriovorus Borrelia burgdorferi Enterococcus faecalis Escherichia coli Bacillus subtilis Campylobacter jejuni Leptospira interrogans Lactococcus lactis Erwinia carotovora Clostridium perfringens Helicobacter pylori Treponema denticola Staphylococcus aureus Fusobacterium nucleatum Lactobacillus casei Helicobacter hepaticum Treponema pallidum Staphylococcus epidermidis Pseudomonas aeruginosa Listeria monocytogenes Vibrio cholerae Streptococcus mutans Rickettsia prowazekii Streptomyces coelicolor Vibrio parahaemolyticus Streptococcus pneumoniae Salmonella enterica Yersinia pestis mre-like genes have been identified in a wide variety of prokaryotes, including eubacteria and archaea (see examples in Table 1). The mrebcd genes of the Grampositive bacterium B. subtilis are present in the divivb operon, along with the mincd minicell genes (Fig. 1; Levin et al., 1992; Varley and Stewart, 1992). An mrec gene has been identified in over 150 different species of Grampositive and Gram-negative bacteria, including bacilli, cocci and spiral shaped cells. MreB-encoding determinants are conspicuously absent from coccoid species. B. subtilis, as well as other species in this genus, is unusual in that it carries three genes with sequence similarity to the E. coli mreb gene: mreb (part of the divivb operon), mbl (for mreb-like) and mrebh [K. Kobayashi, T. Sato and Y. Kobayashi (1994), GenBank Accession Number D37799; Abhayawardhane and Stewart, 1995]. Although the early work on the mre genes was carried out with E. coli, much of the recent work has been accomplished using B. subtilis. MreB is a -associated protein. Immunofluorescence studies revealed that it assembles into transverse bands, reminiscent of the cell division proteins such as FtsZ that assemble into a ring structure at the site of septum formation. The major observed difference between MreB and FtsZ rings is that the former has a helical slant, rather than being perpendicular to the long axis of the cell like FtsZ, and appears to be composed of discontinuous helical coils (Jones et al., 2001; Defeu Soufo and Graumann, 2005). mreb is an essential gene (Formstone and Errington, 2005) encoding a protein with sequence signatures characteristic of proteins in the actin superfamily (Bork et al., 1992). As already mentioned, MreB was proposed to be a negative regulator of FtsI and hence septal peptidoglycan synthesis in E. coli (Wachi and Matsuhashi, 1989), and it is involved in cell width control in B. subtilis (Jones et al., 2001). There is indirect (Lee et al., 2003) and direct (Kruse et al., 2005) evidence that MreB interacts with the MreCD proteins. The Mbl protein is identical at 55% of the amino acid positions with the B. subtilis MreB protein, and the similarity between the two proteins is 79.6% if conservative amino acid substitutions are included in the calculation. The corresponding values for Mbl and E. coli MreB proteins are 54.4% and 79.6% respectively. Thus, the Mbl protein is equally similar to B. subtilis and E. coli MreB, mainly because of the fact that the same or a similar amino acid is found at the same position in all three proteins [138 of the 196 amino acid identities between the B. subtilis and E. coli MreBs are found in Mbl (70.4%) and a further 20 (10.2%) are replaced by similar residues]. The Mbl protein, like its MreB counterpart, is able to assemble into a cytoskeletal structure in B. subtilis cells, although its appearance and function are quite distinct from that of the MreB coil. Mbl assembles into a helical structure that runs the entire length of the cell (Jones et al., 2001). The Mbl polymers are dynamic structures that are remodelled during growth and division (Carballido-López and Errington, 2003). Mbl has been proposed to function as a controller of the linear axis of the cell (Jones et al., 2001). It is interesting that incorporation of new peptidoglycan during lateral wall synthesis in B. subtilis occurs in a helical pattern that resembles the helical pattern of the Mbl filaments (Daniel and Errington, 2003). This suggests that Mbl might form the scaffold on which the lateral wall extension biosynthetic complex assembles and functions. Rod-shaped bacteria lacking MreB homologues do not display the helical pattern of peptidoglycan synthesis but, instead, incorporate new peptidoglycan only at the poles, suggesting that they are restricted to septum-only peptidoglycan synthesis P divivb B. subtilis divivb operon mreb mrec mred minc mind 35.9 kda peripheral protein 32.1 kda spanning protein with a single trans domain 19.8 kda integral protein cell division inhibitor complex Fig. 1. The divivb operon of B. subtilis. The five genes of the operon are transcribed from a promoter positioned upstream of the mreb determinant (P divivb ).
3 Bacterial morphogenes 1179 (Daniel and Errington, 2003). The structure and function of the third MreB-like protein, MreBH, has not yet been determined. The MreC protein is located in the cytoplasmic, with a short cytoplasmic tail at the N-terminus, a single trans domain, and the majority of the sequence positioned externally to the (Lee et al., 2003; Kruse et al., 2005). Structure predictions for MreC from a variety of bacteria suggest that they have a coiled-coil domain that may be involved in dimerization or multimerization (Kruse et al., 2005). The protein is essential for the viability of B. subtilis and E. coli and its depletion alters the pattern of peptidoglycan synthesis and causes cell lysis (Lee and Stewart, 2003; Kruse et al., 2005; Leaver and Errington, 2005). MreC has been shown to interact with both the MreB and MreD proteins (Lee et al., 2003; Kruse et al., 2005). Interestingly, MreB does not polymerize correctly in E. coli cells depleted of either MreC or MreD, suggesting that the latter are required for correct localization of the MreB filament (Kruse et al., 2005). MreD is a very hydrophobic cytoplasmic protein that is essential for viability and interacts with MreC (Lee et al., 2003; Kruse et al., 2005; Leaver and Errington, 2005). The effects of MreD depletion on MreB in E. coli are similar to those caused by depletion of MreC (Kruse et al., 2005) Limitations and advances in the genetic analysis of the mre system Cell wall biosynthesis is a complex process that is essential for the viability. Because of the interplay of so many proteins, it is difficult to determine the specific function of individual proteins. The fact that the original E. coli mreb and mrebcd mutants were viable led to the assumption that these genes are not essential. The discovery that the mre genes were essential in B. subtilis generated considerable futile debate about why these determinants might be more critical in the context of a Gram-positive cell envelope. It has now been established that the mrebcd genes are essential for viability in E. coli (Kruse et al., 2005), the original mutants having undoubtedly acquired suppressor mutations that have led to the stable, viable phenotype. This is a major limitation of genetic analysis of these genes. Mutations affecting these loci generate strong selective pressures for secondary mutations. Thus, the resulting phenotype is not solely the result of the mutation in the essential gene, but a consequence of that mutation plus any number of suppressor mutations in unidentified (but potentially interesting) genes that have arisen during the cultivation of the mutant strain. Because of the essential nature of the mre genes, genetic studies often involve the use of inducible gene constructs. Cells are grown in the presence of the inducer to maintain cell viability but can be washed free of the inducer and cultured under non-inducing conditions to examine the effects of depletion of the protein on viability and morphology. However, the level of protein produced under fully induced conditions might differ from those normally produced. Thus, the production of abnormally low levels of a particular protein might put selective pressure on the cells, resulting in selection of suppressor mutations. Conversely, excessive protein production might negatively impact the regulatory network. Furthermore, the exogenous promoter might be leaky, raising questions about whether the resulting phenotype is the same as when the protein is completely absent. The morphological changes associated with loss of a cell shape determinant also confound the interpretation of results. When gene inactivation results in gross morphological alteration in the cell, other components of the cell wall biosynthetic might not localize or function correctly. Is this due to loss of the gene product or to altered cell geometry? Is the observed phenotype due to the loss of the protein or, more likely, a consequence of a global breakdown in the network? The environment also impacts the cell morphologies obtained. MreC depletion results in cell wall defects that lead to defects in the permeability barrier (Lee and Stewart, 2003). As the cells swell, physical stresses increase their diameter and cause them to twist. Their viability can be improved by making the culture medium isotonic with the cytoplasm of the cells. This produces a spherical phenotype in the MreC-depleted cells. Errington and coworkers have discovered that elevated levels of magnesium can stabilize and maintain viability of MreC- and MreD-depleted cells and additionally restore the normal morphology to MreB-depleted cells (Formstone and Errington, 2005; Leaver and Errington, 2005). The mechanisms underlying the action of the magnesium are not clear but the elevated cation concentration might somehow stabilize the cell wall structure, as elevated magnesium levels can stabilize cells with mutations in certain cell wall biosynthesis or cell morphology genes (Rogers et al., 1976; Murray et al., 1998). Magnesium supplementation might reduce or eliminate the selective pressure for the suppressor mutations that normally arise in Mre protein-depleted cells. The use of magnesium supplementation allowed Errington and coworkers to create true null mutants in the mre determinants (Formstone and Errington, 2005; Leaver and Errington, 2005). The Oxford team might now be able to use this cleaner genetic background to define more precisely the function of the Mre proteins in cell wall biosynthesis and shape determination. Putting the puzzle together Work with the mre genes in B. subtilis and E. coli has
4 1180 G. C. Stewart c m PG Mbl MreB Fig. 2. Model for the involvement of the Mre proteins in cell wall synthesis in B. subtilis. The Mbl and MreB proteins form helical coils in the cell and contact the cell (cm) at the MreCD complexes. The MreCD complexes form contacts with the penicillinbinding proteins that carry out the synthesis of the cell wall peptidoglycan (PG). MreC trans dimers are depicted in yellow, the integral MreD proteins as pink ovals, PBP 2B as green diamonds, and the other penicillin-binding proteins as red triangles. The interaction of Mbl with the MreCD proteins regulates the activity and spatial configuration of lateral wall extension and the MreB coil is predicted to regulate the switch to septal peptidoglycan synthesis mediated by PBP 2B at the midcell and polar potential division sites. The activity at the polar sites is inhibited by the divivb operon-encoded MinCD septation repressor (not shown). progressed to the point where a clearer picture of the role of these proteins in cell wall biosynthesis is now emerging. Errington and coworkers have shown that the Mbl filaments, the MreCD proteins and nascent cell wall synthesis occur in identical helical patterns. The absence of MreC and MreD results in loss of cell viability, swelling and lysis (Lee and Stewart, 2003; Kruse et al., 2005; Leaver and Errington, 2005). A model can now be proposed to explain the experimental observations (Fig. 2). MreC (presumably as a dimer) and MreD form the complex essential for coupling Mbl to the cell elongation PBPs. Lateral wall extension is dependent on the signalling of the Mbl protein to the PBPs [as predicted by Leaver and Errington (2005)]. MreB forms a helical ring structure at the three potential division sites in B. subtilis, the midcell site and the two polar sites. MreB also interacts with the MreCD complex (Lee et al., 2003; Kruse et al., 2005). MreB might downregulate PBP 2B septum-specific peptidoglycan synthesis and, thus, permit lateral wall extension mediated by the other PBPs. At the time of cell division, MreB would be involved in the inactivation of lateral wall synthesis and activation of PBP 2B-mediated septum peptidoglycan synthesis. This synthesis normally occurs only at the midcell site because of the septation inhibition at the two polar sites by the divivb operonencoded MinCD proteins. Deletion of MreB disrupts the repression of PBP 2B activity. This would lead to a uniquely septal pattern of cell wall synthesis and, consequently, to loss of lateral wall synthesis (consistent with the two-competing-sites model). Loss of lateral wall synthesis results in a weakening of the lateral wall, loss of osmostability and swelling of the cell (explaining the observed increase in cell diameter) followed by lysis. Loss of MreCD leads to the same end, but by a different mechanism. Here the coupling of Mbl to the PBPs is lost, resulting in a loss of the helical lateral wall extension peptidoglycan synthesis and leaving only septation as a mechanism for wall incorporation. Because the MreCD-Mbl connection is unaffected by MreB deletion, stabilization of the envelope with Mg 2+ leads to normal wall synthesis (or the magnesium inhibits the PBP 2B stimulation). Septal synthesis of peptidoglycan is less dependent on MreCD, although continued survival of the cell requires more than simple osmotic stabilization (Lee and Stewart, 2003; Leaver and Errington, 2005). Much work remains to be done before the predictions of the above model can be verified or eliminated. The nature of the specific interactions among the Mre proteins and the PBPs remains to be determined. The MreB coil does not form in cells lacking MreC or MreD, suggesting that this complex is required for polymerization of MreB (Kruse et al., 2005). It is not known whether this is also true for Mbl or if the MreCD proteins localize correctly in the absence of the MreB or Mbl coils. Localization of PBPs is not dependent on the formation of the MreB or Mbl coils, but their distribution in MreCD-depleted cells has not been examined (Scheffers et al., 2004). How are cell wall biosynthesis regulatory signals generated and transmitted through this complex? How does MreBH fit into this system? And, lastly, why do members of the Bacillus genus possess three MreB-like proteins whereas other rod-shaped bacteria possess only one? The tools are now available to answer these questions. Acknowledgements Work in the Stewart laboratory was supported by Grant GM57049 from the National Institutes of Health. References Abhayawardhane, Y.K., and Stewart, G.C. 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