Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Bacterial cell shape

Key Points

Our understanding of bacterial cell shape has taken steps forward with the recent discovery of cytoskeletal elements such as cell-shape determinants, but there is still much to learn about how shape is generated and maintained.

The bacterial cell wall, with its peptidoglycan layer, has a primary role in maintaining cell shape. The penicillin-binding proteins (PBPs) carry out the reactions for synthesis and remodelling of peptidoglycan. Different PBPs have specific roles in cell division and elongation, and therefore in cell-shape determination.

Growth of the cell wall is not uniform, but is localized to specific regions. These regions of localized peptidoglycan synthesis vary among bacteria and often change during the cell cycle, reflecting different modes of cell growth (longitudinal, septal or polar).

Bacteria have counterparts of all three eukaryotic cytoskeletal protein classes: FtsZ for tubulin, MreB for actin and crescentin for intermediate filament proteins. FtsZ is essential for cell division, MreB is a rod shape determinant and crescentin is required for the curved-rod shape of Caulobacter crescentus. These proteins form internal structures within cells at locations where they are thought to influence peptidoglycan synthesis or remodelling.

Future research on the nature of the peptidoglycan synthesis machinery and its relationship with the bacterial cytoskeleton is key to our understanding of cell-shape generation.

Abstract

Bacterial species have long been classified on the basis of their characteristic cell shapes. Despite intensive research, the molecular mechanisms underlying the generation and maintenance of bacterial cell shape remain largely unresolved. The field has recently taken an important step forward with the discovery that eukaryotic cytoskeletal proteins have homologues in bacteria that affect cell shape. Here, we discuss how a bacterium gains and maintains its shape, the challenges still confronting us and emerging strategies for answering difficult questions in this rapidly evolving field.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Chemistry of peptidoglycan synthesis and processing.
Figure 2: Gram-positive and Gram-negative cell walls.
Figure 3: Where does cell-wall growth occur?
Figure 4: Cytoskeletal elements and cell shape.
Figure 5: Shape information: cytoplasm to cell wall.

References

  1. 1

    Weibull, C. The isolation of protoplasts from Bacillus megaterium by controlled treatment with lysozyme. J. Bacteriol. 66, 688–695 (1953).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. 2

    Lederberg, J. Bacterial protoplasts induced by penicillin. Proc. Natl Acad. Sci. USA 42, 574–577 (1956).

    CAS  PubMed  Google Scholar 

  3. 3

    Weidel, W. & Pelzer, H. Bagshaped macromolecules — a new outlook on bacterial cell walls. Adv. Enzymol. Relat. Areas. Mol. Biol. 26, 193–232 (1964). The first comprehensive review of the bacterial cell wall, this paper introduced now-standard nomenclature such as 'murein' and 'sacculus'.

    Google Scholar 

  4. 4

    Weidel, W., Frank, H. & Martin, H. H. The rigid layer of the cell wall of Escherichia coli strain B. J. Gen. Microbiol. 22, 158–166 (1960).

    CAS  PubMed  Google Scholar 

  5. 5

    Schwarz, U. & Leutgeb, W. Morphogenetic aspects of murein structure and biosynthesis. J. Bacteriol. 106, 588–595 (1971).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Spratt, B. G. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl Acad. Sci. USA 72, 2999–3003 (1975).

    CAS  PubMed  Google Scholar 

  7. 7

    Tamaki, S., Matsuzawa, H. & Matsuhashi, M. Cluster of mrdA and mrdB genes responsible for the rod shape and mecillinam sensitivity of Escherichia coli. J. Bacteriol. 141, 52–57 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. 8

    Nelson, D. E. & Young, K. D. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J. Bacteriol. 182, 1714–1721 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Meberg, B. M., Paulson, A. L., Priyadarshini, R. & Young, K. D. Endopeptidase penicillin-binding proteins 4 and 7 play auxiliary roles in determining uniform morphology of Escherichia coli. J. Bacteriol. 186, 8326–8336 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. 10

    Karamata, D., McConnell, M. & Rogers, H. J. Mapping of rod mutants of Bacillus subtilis. J. Bacteriol. 111, 73–79 (1972).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Rogers, H. J., McConnell, M. & Burdett, I. D. The isolation and characterization of mutants of Bacillus subtilis and Bacillus licheniformis with disturbed morphology and cell division. J. Gen. Microbiol. 61, 155–171 (1970).

    CAS  PubMed  Google Scholar 

  12. 12

    Wagner, P. M. & Stewart, G. C. Role and expression of the Bacillus subtilis rodC operon. J. Bacteriol. 173, 4341–4346 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Levin, P. A., Margolis, P. S., Setlow, P., Losick, R. & Sun, D. Identification of Bacillus subtilis genes for septum placement and shape determination. J. Bacteriol. 174, 6717–6728 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Doi, M. et al. Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells. J. Bacteriol. 170, 4619–4624 (1988). Identification of the MreB protein and its gene sequence, connecting it with cell-shape determination.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Wachi, M. et al. Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli. J. Bacteriol. 169, 4935–4940 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    Varley, A. W. & Stewart, G. C. The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants. J. Bacteriol. 174, 6729–6742 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Matsuzawa, H., Hayakawa, K., Sato, T. & Imahori, K. Characterization and genetic analysis of a mutant of Escherichia coli K-12 with rounded morphology. J. Bacteriol. 115, 436–442 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

    van den Ent, F., Amos, L. A. & Löwe, J. Prokaryotic origin of the actin cytoskeleton. Nature 413, 39–44 (2001). Shows the X-ray crystal structure of MreB as well as its in vitro filament formation, comparing it to actin.

    CAS  PubMed  Google Scholar 

  19. 19

    Jones, L. J., Carballido-Lopez, R. & Errington, J. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104, 913–922 (2001). Reveals the helical structures formed by MreB and Mbl within B. subtilis cells, indicating a cytoskeletal function.

    CAS  PubMed  Google Scholar 

  20. 20

    Bork, P., Sander, C. & Valencia, A. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl Acad. Sci. USA 89, 7290–7294 (1992).

    CAS  PubMed  Google Scholar 

  21. 21

    Kruse, T., Møller-Jensen, J., Løbner-Olesen, A. & Gerdes, K. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J. 22, 5283–5292 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Figge, R. M., Divakaruni, A. V. & Gober, J. W. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51, 1321–1332 (2004).

    CAS  PubMed  Google Scholar 

  23. 23

    Shih, Y. L., Le, T. & Rothfield, L. Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc. Natl Acad. Sci. USA 100, 7865–7870 (2003).

    CAS  PubMed  Google Scholar 

  24. 24

    Ausmees, N., Kuhn, J. R. & Jacobs-Wagner, C. The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115, 705–713 (2003). Presents crescentin as a cell shape determinant in C. crescentus and as an intermediate filament-like protein.

    CAS  PubMed  Google Scholar 

  25. 25

    Mobley, H. L., Koch, A. L., Doyle, R. J. & Streips, U. N. Insertion and fate of the cell wall in Bacillus subtilis. J. Bacteriol. 158, 169–179 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Daniel, R. A. & Errington, J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113, 767–776 (2003). Using fluorescent vancomycin staining in B. subtilis , this study shows helical patterns of peptidoglycan insertion in the presence of Mbl and polar peptidoglycan insertion in the absence of Mbl.

    CAS  PubMed  Google Scholar 

  27. 27

    De Pedro, M. A., Schwarz, H. & Koch, A. L. Patchiness of murein insertion into the sidewall of Escherichia coli. Microbiology 149, 1753–1761 (2003).

    CAS  PubMed  Google Scholar 

  28. 28

    Schlaeppi, J. M., Schaefer, O. & Karamata, D. Cell wall and DNA cosegregation in Bacillus subtilis studied by electron microscope autoradiography. J. Bacteriol. 164, 130–135 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Schlaeppi, J. M., Pooley, H. M. & Karamata, D. Identification of cell wall subunits in Bacillus subtilis and analysis of their segregation during growth. J. Bacteriol. 149, 329–337 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30

    Costa, K. et al. The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J. Bacteriol. 181, 3710–3715 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    Henriques, A. O., Glaser, P., Piggot, P. J. & Moran, C. P. Jr. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 28, 235–247 (1998).

    CAS  PubMed  Google Scholar 

  32. 32

    Labischinski, H., Barnickel, G., Bradaczek, H. & Giesbrecht, P. On the secondary and tertiary structure of murein. Low and medium-angle X-ray evidence against chitin-based conformations of bacterial peptidoglycan. Eur. J. Biochem. 95, 147–155 (1979).

    CAS  PubMed  Google Scholar 

  33. 33

    Bhavsar, A. P., Erdman, L. K., Schertzer, J. W. & Brown, E. D. Teichoic acid is an essential polymer in Bacillus subtilis that is functionally distinct from teichuronic acid. J. Bacteriol. 186, 7865–7873 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Braun, V. Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim. Biophys. Acta 415, 335–377 (1975).

    CAS  PubMed  Google Scholar 

  35. 35

    Braun, V. & Rehn, K. Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur. J. Biochem. 10, 426–438 (1969).

    CAS  PubMed  Google Scholar 

  36. 36

    Belaaouaj, A., Kim, K. S. & Shapiro, S. D. Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase. Science 289, 1185–1188 (2000).

    CAS  PubMed  Google Scholar 

  37. 37

    Ohara, M., Wu, H. C., Sankaran, K. & Rick, P. D. Identification and characterization of a new lipoprotein, NlpI, in Escherichia coli K-12. J. Bacteriol. 181, 4318–4325 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38

    Sonntag, I., Schwarz, H., Hirota, Y. & Henning, U. Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J. Bacteriol. 136, 280–285 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39

    Vollmer, W. & Höltje, J. V. The architecture of the murein (peptidoglycan) in Gram-negative bacteria: vertical scaffold or horizontal layer(s)? J. Bacteriol. 186, 5978–5987 (2004). Reviews the main hypotheses regarding the orientation of glycan strands in Gram-negative peptidoglycan, discussing relevant experimental data.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40

    Yao, X., Jericho, M., Pink, D. & Beveridge, T. Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy. J. Bacteriol. 181, 6865–6875 (1999). Uses AFM as a means to directly measure the mechanical properties of isolated peptidoglycan sacculi.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41

    Dmitriev, B. A., Toukach, F. V., Holst, O., Rietschel, E. T. & Ehlers, S. Tertiary structure of Staphylococcus aureus cell wall murein. J. Bacteriol. 186, 7141–7148 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42

    Dmitriev, B. A. et al. Tertiary structure of bacterial murein: the scaffold model. J. Bacteriol. 185, 3458–3468 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43

    Koch, A. L. & Doyle, R. J. Inside-to-outside growth and turnover of the wall of Gram-positive rods. J. Theor. Biol. 117, 137–157 (1985).

    CAS  PubMed  Google Scholar 

  44. 44

    Labischinski, H., Goodell, E. W., Goodell, A. & Hochberg, M. L. Direct proof of a “more-than-single-layered” peptidoglycan architecture of Escherichia coli W7: a neutron small-angle scattering study. J. Bacteriol. 173, 751–756 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45

    Park, J. T. & Burman, L. G. Elongation of the murein sacculus of Escherichia coli. Ann. Inst. Pasteur. Microbiol. 136A, 51–58 (1985).

    CAS  PubMed  Google Scholar 

  46. 46

    Höltje, J. -V. in Bacterial Growth and Lysis (eds de Pedro, M. A., Höltje, J.-V., Löffelhardt, W.) 419–426 (Plenum Press, New York, 1993).

    Google Scholar 

  47. 47

    Doyle, R. J. & Marquis, R. E. Elastic, flexible peptidoglycan and bacterial cell wall properties. Trends Microbiol. 2, 57–60 (1994).

    CAS  PubMed  Google Scholar 

  48. 48

    Marquis, R. E. Salt-induced contraction of bacterial cell walls. J. Bacteriol. 95, 775–781 (1968).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49

    Koch, A. L. & Woeste, S. Elasticity of the sacculus of Escherichia coli. J. Bacteriol. 174, 4811–4819 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50

    Boulbitch, A., Quinn, B. & Pink, D. Elasticity of the rod-shaped Gram-negative eubacteria. Phys. Rev. Lett. 85, 5246–5249 (2000).

    CAS  PubMed  Google Scholar 

  51. 51

    de Pedro, M. A., Quintela, J. C., Höltje, J. V. & Schwarz, H. Murein segregation in Escherichia coli. J. Bacteriol. 179, 2823–2834 (1997). Localizes regions of peptidoglycan synthesis in E. coli using D -cysteine labelling.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. 52

    Pinho, M. G. & Errington, J. Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol. Microbiol. 50, 871–881 (2003).

    CAS  PubMed  Google Scholar 

  53. 53

    Morlot, C., Zapun, A., Dideberg, O. & Vernet, T. Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Mol. Microbiol. 50, 845–855 (2003).

    CAS  PubMed  Google Scholar 

  54. 54

    Cole, R. M. & Hahn, J. J. Cell wall replication in Streptococcus pyogenes. Science 135, 722–724 (1962).

    CAS  Google Scholar 

  55. 55

    Briles, E. B. & Tomasz, A. Radioautographic evidence for equatorial wall growth in a Gram-positive bacterium. Segregation of choline-3H-labeled teichoic acid. J. Cell. Biol. 47, 786–790 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56

    Young, K. D. Bacterial shape. Mol. Microbiol. 49, 571–580 (2003).

    CAS  PubMed  Google Scholar 

  57. 57

    de Pedro, M. A., Young, K. D., Höltje, J. V. & Schwarz, H. Branching of Escherichia coli cells arises from multiple sites of inert peptidoglycan. J. Bacteriol. 185, 1147–1152 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58

    Graumann, P. L. Cytoskeletal elements in bacteria. Curr. Opin. Microbiol. 7, 565–571 (2004).

    CAS  PubMed  Google Scholar 

  59. 59

    Møller-Jensen, J. & Löwe, J. Increasing complexity of the bacterial cytoskeleton. Curr. Opin. Cell. Biol. 17, 75–81 (2005).

    PubMed  Google Scholar 

  60. 60

    Bi, E. F. & Lutkenhaus, J. FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161–164 (1991). Identifies the FtsZ ring at cell-division sites, implicating it as a possible cytoskeletal element.

    CAS  PubMed  Google Scholar 

  61. 61

    Mukherjee, A., Dai, K. & Lutkenhaus, J. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl Acad. Sci. USA 90, 1053–1057 (1993).

    CAS  PubMed  Google Scholar 

  62. 62

    de Boer, P., Crossley, R. & Rothfield, L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359, 254–256 (1992).

    CAS  PubMed  Google Scholar 

  63. 63

    RayChaudhuri, D. & Park, J. T. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359, 251–254 (1992).

    CAS  PubMed  Google Scholar 

  64. 64

    Bramhill, D. & Thompson, C. M. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc. Natl Acad. Sci. USA 91, 5813–5817 (1994).

    CAS  PubMed  Google Scholar 

  65. 65

    Mukherjee, A. & Lutkenhaus, J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacteriol. 176, 2754–2758 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. 66

    Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199–203 (1998).

    CAS  Google Scholar 

  67. 67

    Löwe, J. & Amos, L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203–206 (1998).

    PubMed  Google Scholar 

  68. 68

    Errington, J., Daniel, R. A. & Scheffers, D. J. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52–65 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69

    Addinall, S. G. & Lutkenhaus, J. FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol. Microbiol. 22, 231–237 (1996).

    CAS  PubMed  Google Scholar 

  70. 70

    Varma, A. & Young, K. D. FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J. Bacteriol. 186, 6768–6774 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71

    Bi, E. & Lutkenhaus, J. Isolation and characterization of ftsZ alleles that affect septal morphology. J. Bacteriol. 174, 5414–5423 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72

    Anderson, D. E., Gueiros-Filho, F. J. & Erickson, H. P. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186, 5775–5781 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. 73

    Thanedar, S. & Margolin, W. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14, 1167–1173 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 74

    Abhayawardhane, Y. & Stewart, G. C. Bacillus subtilis possesses a second determinant with extensive sequence similarity to the Escherichia coli mreB morphogene. J. Bacteriol. 177, 765–773 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. 75

    Defeu Soufo, H. J. & Graumann, P. L. Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep. 5, 789–794 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76

    Defeu Soufo, H. J. & Graumann, P. L. Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr. Biol. 13, 1916–1920 (2003).

    CAS  Google Scholar 

  77. 77

    Carballido-Lopez, R. & Errington, J. The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev. Cell. 4, 19–28 (2003).

    CAS  PubMed  Google Scholar 

  78. 78

    Wortinger, M. A., Quardokus, E. M. & Brun, Y. V. Morphological adaptation and inhibition of cell division during stationary phase in Caulobacter crescentus. Mol. Microbiol. 29, 963–973 (1998).

    CAS  PubMed  Google Scholar 

  79. 79

    Vollmer, W., von Rechenberg, M. & Höltje, J. V. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol. Chem. 274, 6726–6734 (1999).

    CAS  PubMed  Google Scholar 

  80. 80

    Schiffer, G. & Höltje, J. V. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J. Biol. Chem. 274, 32031–32039 (1999).

    CAS  PubMed  Google Scholar 

  81. 81

    Romeis, T. & Höltje, J. V. Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylase in Escherichia coli. J. Biol. Chem. 269, 21603–21607 (1994).

    CAS  PubMed  Google Scholar 

  82. 82

    Alaedini, A. & Day, R. A. Identification of two penicillin-binding multienzyme complexes in Haemophilus influenzae. Biochem. Biophys. Res. Commun. 264, 191–195 (1999). Presents the first experimental evidence that there are multiple peptidoglycan synthesis complexes that differ in the transglycosylase present.

    CAS  PubMed  Google Scholar 

  83. 83

    Weiss, D. S. et al. Localization of the Escherichia coli cell division protein Ftsl (PBP3) to the division site and cell pole. Mol. Microbiol. 25, 671–681 (1997).

    CAS  PubMed  Google Scholar 

  84. 84

    Iwaya, M., Jones, C. W., Khorana, J. & Strominger, J. L. Mapping of the mecillinam-resistant, round morphological mutants of Escherichia coli. J. Bacteriol. 133, 196–202 (1978).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. 85

    Boyle, D. S., Khattar, M. M., Addinall, S. G., Lutkenhaus, J. & Donachie, W. D. ftsW is an essential cell-division gene in Escherichia coli. Mol. Microbiol. 24, 1263–1273 (1997).

    CAS  PubMed  Google Scholar 

  86. 86

    Ikeda, M. et al. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J. Bacteriol. 171, 6375–6378 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. 87

    Hara, H., Yasuda, S., Horiuchi, K. & Park, J. T. A promoter for the first nine genes of the Escherichia coli mra cluster of cell division and cell envelope biosynthesis genes, including ftsI and ftsW. J. Bacteriol. 179, 5802–5811 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. 88

    Matsuzawa, H. et al. Nucleotide sequence of the rodA gene, responsible for the rod shape of Escherichia coli: rodA and the pbpA gene, encoding penicillin-binding protein 2, constitute the rodA operon. J. Bacteriol. 171, 558–560 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. 89

    Ishino, F. et al. Peptidoglycan synthetic activities in membranes of Escherichia coli caused by overproduction of penicillin-binding protein 2 and rodA protein. J. Biol. Chem. 261, 7024–7031 (1986).

    CAS  PubMed  Google Scholar 

  90. 90

    Mercer, K. L. & Weiss, D. S. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J. Bacteriol. 184, 904–912 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91

    Lee, J. C. & Stewart, G. C. Essential nature of the mreC determinant of Bacillus subtilis. J. Bacteriol. 185, 4490–4498 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. 92

    Kruse, T., Bork-Jensen, J. & Gerdes, K. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol. Microbiol. 55, 78–89 (2005).

    CAS  PubMed  Google Scholar 

  93. 93

    Defeu Soufo, H. J. & Graumann, P. L. 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 (2005).

    PubMed  PubMed Central  Google Scholar 

  94. 94

    Scheffers, D. J., Jones, L. J. & Errington, J. Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol. Microbiol. 51, 749–764 (2004).

    CAS  PubMed  Google Scholar 

  95. 95

    Datta, P., Dasgupta, A., Bhakta, S. & Basu, J. Interaction between FtsZ and FtsW of Mycobacterium tuberculosis. J. Biol. Chem. 277, 24983–24987 (2002).

    CAS  PubMed  Google Scholar 

  96. 96

    Nelson, D. E. & Young, K. D. Contributions of PBP 5 and DD-carboxypeptidase penicillin binding proteins to maintenance of cell shape in Escherichia coli. J. Bacteriol. 183, 3055–3064 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. 97

    McPherson, D. C. & Popham, D. L. Peptidoglycan synthesis in the absence of class A penicillin-binding proteins in Bacillus subtilis. J. Bacteriol. 185, 1423–1431 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. 98

    Firtel, M., Henderson, G. & Sokolov, I. Nanosurgery: observation of peptidoglycan strands in Lactobacillus helveticus cell walls. Ultramicroscopy 101, 105–109 (2004).

    CAS  PubMed  Google Scholar 

  99. 99

    Chen, Y. & Erickson, H. P. Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J. Biol. Chem. 280, 22549–22554 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. 100

    Esue, O., Cordero, M., Wirtz, D. & Tseng, Y. The assembly of MreB, a prokaryotic homolog of actin. J. Biol. Chem. 280, 2628–2635 (2005).

    CAS  PubMed  Google Scholar 

  101. 101

    Umeda, A. & Amako, K. Growth of the surface of Corynebacterium diphtheriae. Microbiol. Immunol. 27, 663–671 (1983).

    CAS  PubMed  Google Scholar 

  102. 102

    Motaleb, M. A. et al. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl Acad. Sci. USA 97, 10899–10904 (2000).

    CAS  PubMed  Google Scholar 

  103. 103

    Gitai, Z., Dye, N. A., Reisenauer, A., Wachi, M. & Shapiro, L. MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120, 329–341 (2005). Provides genetic evidence that the drug A22 targets MreB in C. crescentus.

    CAS  PubMed  Google Scholar 

  104. 104

    Trachtenberg, S. Mollicutes-wall-less bacteria with internal cytoskeletons. J. Struct. Biol. 124, 244–256 (1998).

    CAS  PubMed  Google Scholar 

  105. 105

    Kessel, M., Peleg, I., Muhlrad, A. & Kahane, I. Cytoplasmic helical structure associated with Acholeplasma laidlawii. J. Bacteriol. 147, 653–659 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. 106

    Hegermann, J., Herrmann, R. & Mayer, F. Cytoskeletal elements in the bacterium Mycoplasma pneumoniae. Naturwissenschaften 89, 453–458 (2002).

    CAS  PubMed  Google Scholar 

  107. 107

    Williamson, D. L., Renaudin, J. & Bove, J. M. Nucleotide sequence of the Spiroplasma citri fibril protein gene. J. Bacteriol. 173, 4353–4362 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. 108

    Kürner, J., Frangakis, A. S. & Baumeister, W. Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307, 436–438 (2005).

    PubMed  Google Scholar 

  109. 109

    Trachtenberg, S. & Gilad, R. A bacterial linear motor: cellular and molecular organization of the contractile cytoskeleton of the helical bacterium Spiroplasma melliferum BC3. Mol. Microbiol. 41, 827–848 (2001).

    CAS  PubMed  Google Scholar 

  110. 110

    Fraser, C. M. et al. The minimal gene complement of Mycoplasma genitalium. Science 270, 397–403 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. 111

    Wang, X. & Lutkenhaus, J. Characterization of the ftsZ gene from Mycoplasma pulmonis, an organism lacking a cell wall. J. Bacteriol. 178, 2314–2319 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. 112

    Löwe, J., van den Ent, F. & Amos, L. A. Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33, 177–198 (2004).

    PubMed  Google Scholar 

  113. 113

    Ishino, F., Mitsui, K., Tamaki, S. & Matsuhashi, M. Dual enzyme activities of cell wall peptidoglycan synthesis, peptidoglycan transglycosylase and penicillin-sensitive transpeptidase, in purified preparations of Escherichia coli penicillin-binding protein 1A. Biochem. Biophys. Res. Commun. 97, 287–293 (1980).

    CAS  PubMed  Google Scholar 

  114. 114

    Nakagawa, J., Tamaki, S., Tomioka, S. & Matsuhashi, M. Functional biosynthesis of cell wall peptidoglycan by polymorphic bifunctional polypeptides. Penicillin-binding protein 1Bs of Escherichia coli with activities of transglycosylase and transpeptidase. J. Biol. Chem. 259, 13937–13946 (1984).

    CAS  PubMed  Google Scholar 

  115. 115

    Spratt, B. G. & Pardee, A. B. Penicillin-binding proteins and cell shape in E. coli. Nature 254, 516–517 (1975).

    CAS  PubMed  Google Scholar 

  116. 116

    Adam, M. et al. The bimodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes peptide bond formation from thiolesters and does not catalyze glycan chain polymerization from the lipid II intermediate. J. Bacteriol. 179, 6005–6009 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  117. 117

    Spratt, B. G. Temperature-sensitive cell division mutants of Escherichia coli with thermolabile penicillin-binding proteins. J. Bacteriol. 131, 293–305 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. 118

    Korat, B., Mottl, H. & Keck, W. Penicillin-binding protein 4 of Escherichia coli: molecular cloning of the dacB gene, controlled overexpression, and alterations in murein composition. Mol. Microbiol. 5, 675–684 (1991).

    CAS  PubMed  Google Scholar 

  119. 119

    Broome-Smith, J. K., Ioannidis, I., Edelman, A. & Spratt, B. G. Nucleotide sequences of the penicillin-binding protein 5 and 6 genes of Escherichia coli. Nucleic Acids Res. 16, 1617 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 120

    Baquero, M. R., Bouzon, M., Quintela, J. C., Ayala, J. A. & Moreno, F. dacD, an Escherichia coli gene encoding a novel penicillin-binding protein (PBP6b) with DD-carboxypeptidase activity. J. Bacteriol. 178, 7106–7111 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  121. 121

    Romeis, T. & Höltje, J. V. Penicillin-binding protein 7/8 of Escherichia coli is a DD-endopeptidase. Eur. J. Biochem. 224, 597–604 (1994).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Owing to space constraints, we were forced to eliminate references to many papers that we feel have contributed valuable ideas and data to the field and to our review. We extend our sincerest apologies to the authors of these papers. The authors are grateful to members of the Jacobs-Wagner laboratory for critical reading of the manuscript. Research in our laboratory is funded by the National Institutes of Health and by the Pew Scholars Programme in the Biological Sciences, sponsored by the Pew Charitable Trusts.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Christine Jacobs-Wagner.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Related links

Related links

DATABASES

Entrez

Bacillus subtilis

B. subtilis mreB

Borrelia burgdorferi

Caulobacter crescentus

Escherichia coli

E. coli mreB

ftsI

Haemophilus influenzae

Helicobacter pylori

mbl

mreBH

Mycobacterium tuberculosis

Mycoplasma genitalium

Mycoplasma pneumoniae

pbpA

Staphylococcus aureus

SwissProt

B. subtilis MreB

Crescentin

Mbl

MipA

MltA

MreBH

SpoVE

FURTHER INFORMATION

The Jacobs-Wagner laboratory

Glossary

PEPTIDOGLYCAN

A covalently linked macromolecular structure made up of stiff glycan strands crosslinked by somewhat flexible peptide bridges. It gives the cell wall its strength. Also called 'murein', from Latin murus, wall.

SACCULUS

A synonym for the 'sac-like' peptidoglycan molecule that surrounds the cytoplasmic membrane of a bacterium.

SPHEROPLAST

A cell in which the cell wall is either absent or disrupted, causing it to adopt a spherical shape.

PENICILLIN-BINDING PROTEINS

A class of enzymes first discovered by their ability to bind labelled penicillin. They catalyse the reactions that are necessary to synthesize and modify peptidoglycan.

TEICHOIC ACIDS

Phosphate-rich, anionic polysaccharides that are attached to the peptidoglycan of Gram-positive bacteria. In Bacillus subtilis, most are polyglycerol phosphate or polyribitol phosphate and, in the case of lipoteichoic acids, have lipid modifications that allow association with the cytoplasmic membrane.

TRANSGLYCOSYLASE

An enzyme that catalyses the attachment of a peptidoglycan disaccharide-pentapeptide precursor molecule to an existing glycan strand by a β-1,4 glycosidic bond.

TRANSPEPTIDASE

An enzyme that catalyses the formation of a peptide bond between adjacent polypeptide side chains, forming a flexible peptide bridge between glycan strands.

PEPTIDE INTERBRIDGE

Additional amino acids that bridge the D-alanine in position 4 from one peptide with the dibasic amino acid in position 3 of the adjacent peptide. In the Gram-positive bacterium Staphylococcus aureus, for example, interbridges comprise five glycine residues.

PEPTIDOGLYCAN HYDROLASES

A class of enzymes that break molecular bonds in peptidoglycan. They are required to allow insertion of new peptidoglycan and to enable cell division, but must be tightly regulated to prevent autolysis.

ATOMIC FORCE MICROSCOPY

A technique in which a sharp tip is scanned across the surface of a sample, probing sample-tip interaction forces. The resulting 'image' is high resolution and, as no light is required, the sample can be hydrated in aqueous solutions.

MIN

The Min system comprises three proteins in Escherichia coli: MinC, MinD and MinE. Mutations in the min genes produce characteristic mini cells. The cooperative action of MinC, MinD and MinE proteins ensures the placement of the division site at the midcell.

Z RING

The ring-shaped structure that is formed during cell division from FtsZ polymers. The Z ring recruits proteins that are required for septal wall synthesis and cell division.

VANCOMYCIN

An antibiotic that binds to the C-terminal D-alanine–D-alanine polypeptide of peptidoglycan precursors, preventing the transpeptidation reaction that is required for peptide crosslinking of glycan strands.

MOLLICUTES

A class of wall-less bacteria that includes acholeplasmas, mycoplasmas and spiroplasmas. They have the simplest genomes of any self-replicating, free-living organisms but can retain defined shapes by virtue of internal cytoskeletons.

CRYO-ELECTRON TOMOGRAPHY

A technique in which a specimen, embedded in vitreous ice, is imaged from multiple angles using electron microscopy. The resulting images are then combined to reconstruct the 3D structure of the specimen.

OPERONIC

Describes multiple genes in an operon, a single transcriptional unit driven by a single promoter. Operons often contain genes encoding protein products that act in the same pathway.

MONOCISTRONIC

Transcribed as a single gene.

LYTIC TRANSGLYCOSYLASE

An enzyme that cleaves the bonds between adjacent aminosugar moieties in glycan strands of peptidoglycan, enabling new precursor molecules to be added.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cabeen, M., Jacobs-Wagner, C. Bacterial cell shape. Nat Rev Microbiol 3, 601–610 (2005). https://doi.org/10.1038/nrmicro1205

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing