1887

Abstract

The prokaryotic cytoskeletal protein MreB is thought to govern cell shape by positioning the cell wall synthetic apparatus at growth sites in the cell. In rod-shaped bacteria it forms helical filaments that run around the periphery of the rod during elongation. Gram-positive bacteria often contain more than one gene. has three -like genes, , and , the first two of which have been shown to be essential under normal growth conditions. Expression of an homologue from the closely related organism did not have any effect on cell growth or morphology. In contrast, expression of from the phylogenetically more distant bacterium produced shape defects and ultimately cell death, due to disruption of the endogenous MreB cytoskeleton. However, expression of either () or () was sufficient to confer a rod shape to deleted for the three isologues, supporting the idea that the three proteins have largely redundant functions in cell morphogenesis. Expression of could fully compensate for the loss of in and led to the formation of rod-shaped cells. In contrast, expression of was not sufficient to confer a rod shape to Δ, indicating that a complex of these three cell shape determinants is not enough for cell morphogenesis of .

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2009-11-01
2020-01-22
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References

  1. Abhayawardhane, Y. & Stewart, G. C. ( 1995; ). Bacillus subtilis possesses a second determinant with extensive sequence similarity to the Escherichia coli mreB morphogene. J Bacteriol 177, 765–773.
    [Google Scholar]
  2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  3. Alyahya, S. A., Alexander, R., Costa, T., Henriques, A. O., Emonet, T. & Jacobs-Wagner, C. ( 2009; ). RodZ, a component of the bacterial core morphogenic apparatus. Proc Natl Acad Sci U S A 106, 1239–1244.[CrossRef]
    [Google Scholar]
  4. Anagnostopoulos, C. & Spizizen, J. ( 1961; ). Requirements for transformation in Bacillus subtilis. J Bacteriol 81, 741–746.
    [Google Scholar]
  5. Bendezu, F. O., Hale, C. A., Bernhardt, T. G. & de Boer, P. A. ( 2009; ). RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. EMBO J 28, 193–204.[CrossRef]
    [Google Scholar]
  6. Bork, P., Sander, C. & Valencia, A. ( 1992; ). An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci U S A 89, 7290–7294.[CrossRef]
    [Google Scholar]
  7. Carballido-Lopez, R. ( 2006a; ). Orchestrating bacterial cell morphogenesis. Mol Microbiol 60, 815–819.[CrossRef]
    [Google Scholar]
  8. Carballido-López, R. ( 2006b; ). The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev 70, 888–909.[CrossRef]
    [Google Scholar]
  9. Carballido-López, R., Formstone, A., Li, Y., Ehrlich, S. D., Noirot, P. & Errington, J. ( 2006; ). Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 11, 399–409.[CrossRef]
    [Google Scholar]
  10. Daniel, R. A. & Errington, J. ( 2003; ). Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113, 767–776.[CrossRef]
    [Google Scholar]
  11. Defeu Soufo, H. J. & Graumann, P. L. ( 2005; ). Bacillus subtilis actin-like protein MreB influences the positioning of the replication machinery and requires membrane proteins MreC/D and other actin-like proteins for proper localization. BMC Cell Biol 6, 10 [CrossRef]
    [Google Scholar]
  12. Defeu Soufo, H. J. & Graumann, P. L. ( 2006; ). Dynamic localization and interaction with other Bacillus subtilis actin-like proteins are important for the function of MreB. Mol Microbiol 62, 1340–1356.[CrossRef]
    [Google Scholar]
  13. Figge, R. M., Divakaruni, A. V. & Gober, J. W. ( 2004; ). MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51, 1321–1332.[CrossRef]
    [Google Scholar]
  14. Formstone, A. & Errington, J. ( 2005; ). A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis. Mol Microbiol 55, 1646–1657.[CrossRef]
    [Google Scholar]
  15. Glaser, P., Sharpe, M. E., Raether, B., Perego, M., Ohlsen, K. & Errington, J. ( 1997; ). Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev 11, 1160–1168.[CrossRef]
    [Google Scholar]
  16. Hayhurst, E. J., Kailas, L., Hobbs, J. K. & Foster, S. J. ( 2008; ). Cell wall peptidoglycan architecture in Bacillus subtilis. Proc Natl Acad Sci U S A 105, 14603–14608.[CrossRef]
    [Google Scholar]
  17. Jenkinson, H. F. ( 1983; ). Altered arrangement of proteins in the spore coat of a germination mutant of Bacillus subtilis. J Gen Microbiol 129, 1945–1958.
    [Google Scholar]
  18. Jones, L. J., Carballido-López, R. & Errington, J. ( 2001; ). Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104, 913–922.[CrossRef]
    [Google Scholar]
  19. Kawai, Y., Daniel, R. A. & Errington, J. ( 2009a; ). Regulation of cell wall morphogenesis in Bacillus subtilis by recruitment of PBP1 to the MreB helix. Mol Microbiol 71, 1131–1144.[CrossRef]
    [Google Scholar]
  20. Kawai, Y., Asai, K. & Errington, J. ( 2009b; ). Partial functional redundancy of MreB isoforms, MreB, Mbl and MreBH, in cell morphogenesis of Bacillus subtilis. Mol Microbiol 73, 719–731.[CrossRef]
    [Google Scholar]
  21. Kruse, T., Bork-Jensen, J. & Gerdes, K. ( 2005; ). The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55, 78–89.
    [Google Scholar]
  22. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & other authors ( 2007; ). clustal w and clustal x version 2.0. Bioinformatics 23, 2947–2948.[CrossRef]
    [Google Scholar]
  23. Leaver, M. & Errington, J. ( 2005; ). Roles for MreC and MreD proteins in helical growth of the cylindrical cell wall in Bacillus subtilis. Mol Microbiol 57, 1196–1209.[CrossRef]
    [Google Scholar]
  24. Lee, J.-C. & Stewart, G. C. ( 2003; ). Essential nature of the mreC determinant of Bacillus subtilis. J Bacteriol 185, 4490–4498.[CrossRef]
    [Google Scholar]
  25. Nicholson, W. L. & Setlow, P. ( 1990; ). Sporulation, germination and outgrowth. In Molecular Biological Methods for Bacillus, pp. 391–450. Edited by C. R. Harwood & S. M. Cutting. New York: Wiley.
  26. Rogers, H. J. & Taylor, C. ( 1978; ). Autolysins and shape change in rodA mutants of Bacillus subtilis. J Bacteriol 135, 1032–1042.
    [Google Scholar]
  27. Rogers, H. J., McConnell, M. & Burdett, I. D. ( 1970; ). The isolation and characterization of mutants of Bacillus subtilis and Bacillus licheniformis with disturbed morphology and cell division. J Gen Microbiol 61, 155–171.[CrossRef]
    [Google Scholar]
  28. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  29. Schirner, K. & Errington, J. ( 2009; ). Cell wall regulator σ I specifically suppresses the lethal phenotype of mbl mutants in B. subtilis. J Bacteriol 191, 1404–1413.[CrossRef]
    [Google Scholar]
  30. Shiomi, D., Sakai, M. & Niki, H. ( 2008; ). Determination of bacterial rod shape by a novel cytoskeletal membrane protein. EMBO J 27, 3081–3091.[CrossRef]
    [Google Scholar]
  31. Stewart, G. C. ( 2005; ). Taking shape: control of bacterial cell wall biosynthesis. Mol Microbiol 57, 1177–1181.[CrossRef]
    [Google Scholar]
  32. Tiyanont, K., Doan, T., Lazarus, M. B., Fang, X., Rudner, D. Z. & Walker, S. ( 2006; ). Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. Proc Natl Acad Sci U S A 103, 11033–11038.[CrossRef]
    [Google Scholar]
  33. van den Ent, F., Amos, L. A. & Löwe, J. ( 2001; ). Prokaryotic origin of the actin cytoskeleton. Nature 413, 39–44.[CrossRef]
    [Google Scholar]
  34. van den Ent, F., Leaver, M., Bendezu, F., Errington, J., de Boer, P. & Löwe, J. ( 2006; ). Dimeric structure of the cell shape protein MreC and its functional implications. Mol Microbiol 62, 1631–1642.[CrossRef]
    [Google Scholar]
  35. Wachi, M., Doi, M., Okada, Y. & Matsuhashi, M. ( 1989; ). New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells. J Bacteriol 171, 6511–6516.
    [Google Scholar]
  36. Wei, Y., Havasy, T., McPherson, D. C. & Popham, D. L. ( 2003; ). Rod shape determination by the Bacillus subtilis class B penicillin-binding proteins encoded by pbpA and pbpH. J Bacteriol 185, 4717–4726.[CrossRef]
    [Google Scholar]
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