Granular layer in the periplasmic space of gram-positive bacteria and fine structures of Enterococcus gallinarum and Streptococcus gordonii septa revealed by cryo-electron microscopy of vitreous sections

Journal of Bacteriology

Volumn 188, Issue 18, 2006, Pages 6652-6660

  Zuber, Benoît ^a   Haenni, Marisa ^a   Ribeiro, Tânia ^b   Minnig, Kathrin ^a,c   Lopes, Fátima ^b   Moreillon, Philippe ^a   Dubochet, Jacques ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c ZLB Behring AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FTSZ PROTEIN; PEPTIDOGLYCAN;

ARTICLE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIUM CULTURE; CELL DIVISION; CRYOELECTRON MICROSCOPY; CYTOPLASM; ENTEROCOCCUS GALLINARUM; GRAM POSITIVE BACTERIUM; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; STREPTOCOCCUS GORDONII;

BACILLUS SUBTILIS; CELL MEMBRANE; CELL WALL; CRYOELECTRON MICROSCOPY; CRYOULTRAMICROTOMY; CYTOPLASM; CYTOSKELETON; ENTEROCOCCUS; MACROMOLECULAR SUBSTANCES; MODELS, BIOLOGICAL; PEPTIDOGLYCAN; PERIPLASM; STREPTOCOCCUS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ENTEROCOCCUS GALLINARUM; POSIBACTERIA; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS GORDONII;

EID: 33748804439     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00391-06     Document Type: Article

References (46)

1. Al-Amoudi, A., J. J. Chang, A. Leforestier, A. McDowall, L. M. Salamin, L. P. Norlen, K. Richter, N. Sartori Blanc, D. Studer, and J. Dubochet. 2004. Cryo-electron microscopy of vitreous sections. EMBO J. 23:3583-3588.
2. Al-Amoudi, A., L. P. Norlen, and J. Dubochet. 2004. Cryo-electron microscopy of vitreous sections of native biological cells and tissues. J. Struct. Biol. 148:131-135.
3. Beveridge, T. J. 1995. The periplasmic space and the periplasm in gram-positive and gram-negative bacteria. ASM News 61:125-130.
4. Beveridge, T. J. 2000. Ultrastructure of gram-positive cell walls, p. 3-10. In V. A. Fischetti (ed.), Gram-positive pathogens. ASM Press, Washington, D.C.
5. Bi, E. F., and J. Lutkenhaus. 1991. FtsZ ring structure associated with division in Escherichia coli. Nature 354:161-164.
6. Briles, E. B., and A. Tomasz. 1970. Radioautographic evidence for equatorial wall growth in a gram-positive bacterium. Segregation of choline-3H-labeled teichoic acid. Cell Biol. 47:786-790.
7. Daniel, R. A., and J. Errington. 2003. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767-776.
8. Daniel, R. A., E. J. Harry, and J. Errington. 2000. Role of penicillin-binding protein PBP 2B in assembly and functioning of the division machinery of Bacillus subtilis. Mol. Microbiol. 35:299-311.
9. de Gennes, P. G. 1979. Scaling concepts in polymer physics. Cornell University Press, Ithaca, N. Y.
10. Dubochet, J., M. Adrian, J. J. Chang, J. C. Homo, J. Lepault, A. W. McDowall, and P. Schultz. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129-228.
11. Dubochet, J., and N. Sartori Blanc. 2001. The cell in absence of aggregation artifacts. Micron 32:91-99.
12. Eltsov, M., and J. Dubochet. 2005. Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections. J. Bacteriol. 187:8047-8054.
13. Erickson, H. P., D. W. Taylor, K. A. Taylor, and D. Bramhill. 1996. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc. Natl. Acad. Sci. USA 93:519-523.
14. Gould, A. R., B. K. May, and W. H. Elliott. 1975. Release of extracellular enzymes from Bacillus amyloliquefaciens. J. Bacteriol. 122:34-40.
15. Graham, L. L., and T. J. Beveridge. 1994. Structural differentiation of the Bacillus subtilis 168 cell wall. J. Bacteriol. 176:1413-1421.
16. Hsieh, C. E., A. Leith, C. A. Mannella, J. Frank, and M. Marko. 2006. Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections. J. Struct. Biol. 153:1-13.
17. Hsieh, C. E., M. Marko, J. Frank, and C. A. Mannella. 2002. Electron tomographic analysis of frozen-hydrated tissue sections. J. Struct. Biol. 138:63-73.
18. Kawamura, Y., X. G. Hou, F. Sultana, H. Miura, and T. Ezaki. 1995. Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int. J. Syst. Bacteriol. 45:406-408.
19. Koch, A. L. 2003. Were gram-positive rods the first bacteria? Trends Microbiol. 11:166-170.
20. Koch, A. L., and R. J. Doyle. 1985. Inside-to-outside growth and turnover of the wall of gram-positive rods. J. Theor. Biol. 117:137-157.
21. Lim, D., and N. C. Strynadka. 2002. Structural basis for the beta lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus. Nat. Struct. Biol. 9:870-876.
22. Margolin, W. 2005. FtsZ and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6:862-871.
23. Matias, V. R., and T. J. Beveridge. 2005. Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol. Microbiol. 56:240-251.
24. Matias, V. R., and T. J. Beveridge. 2006. Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J. Bacteriol. 188:1011-1021.
25. Merchante, R., H. M. Pooley, and D. Karamata. 1995. A periplasm in Bacillus subtilis. J. Bacteriol. 177:6176-6183.
26. Morlot, C, M. Noirclerc-Savoye, A. Zapun, O. Dideberg, and T. Vernet. 2004. The D,D-carboxypeptidase PBP3 organizes the division process of Streptococcus pneumoniae. Mol. Microbiol. 51:1641-1648.
27. Morlot, G, A. Zapun, O. Dideberg, and T. Vernet. 2003. Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Mol. Microbiol. 50:845-855.
28. Nickell, S., C. Kofler, A. P. Leis, and W. Baumeister. 2006. A visual approach to proteomics. Nat. Rev. Mol. Cell Biol. 7:225-230.
29. Pares, S., N. Mouz, Y. Petillot, R. Hakenbeck, and O. Dideberg. 1996. X-ray structure of Streptococcus pneumoniae PBP2x, a primary penicillin target enzyme. Nat. Struct. Biol. 3:284-289.
30. Paul, T. R., A. Venter, L. C. Blaszczak, T. R. Parr, Jr., H. Labischinski, and T. J. Beveridge. 1995. Localization of penicillin-binding proteins to the splitting system of Staphylococcus aureus septa by using a mercury-penicillin V derivative. J. Bacteriol. 177:3631-3640.
31. Pinho, M. G., and J. Errington. 2003. Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol. Microbiol. 50:871-881.
32. Pinho, M. G., and J. Errington. 2005. Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates. Mol. Microbiol. 55:799-807.
33. Pozzi, G., R. A. Musmanno, P. M.-J. Lievens, M. R. Oggioni, P. Plevani, and R. Manganelli. 1990. Method and parameters for genetic transformation of Streptococcus sanguis Challis. Res. Microbiol. 141:659-670.
34. Richter, K. 1994. A cryoglue to mount vitreous biological specimens for cryoultramicrotomy at 110K. J. Microsc. 173:143-147.
35. Sartori Blanc, N., A. Senn, A. Leforestier, F. Livolant, and J. Dubochet. 2001. DNA in human and stallion spermatozoa forms local hexagonal packing with twist and many defects. J. Struct. Biol. 134:76-81.
36. Scheffers, D. J., L. J. Jones, and J. Errington. 2004. Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol. Microbiol. 51:749-764.
37. Scheffers, D. J., and M. G. Pinho. 2005. Bacterial cell wall synthesis: new insights from localization studies. Microbiol. Mol. Biol. Rev. 69:585-607.
38. Schuster, C., B. Dobrinski, and R. Hakenbeck. 1990. Unusual septum formation in Streptococcus pneumoniae mutants with an alteration in the D,D-carboxypeptidase penicillin-binding protein 3. J. Bacteriol. 172:6499-6505.
39. Seltmann, G., and O. Holst. 2001. The bacterial cell wall. Springer, Berlin, Germany.
40. Shockman, G. D., and J. F. Barrett. 1983. Structure, function, and assembly of cell walls of gram-positive bacteria. Annu. Rev. Microbiol. 37:501-527.
41. Spizizen, J. 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. USA 44:1072-1078.
42. Stock, J. B., B. Rauch, and S. Roseman. 1977. Periplasmic space in Salmonella typhimurium and Escherichia coli. J. Biol. Chem. 252:7850-7861.
43. Tomasz, A., J. D. Jamieson, and E. Ottolenghi. 1964. The fine structure of Diplococcus pneumoniae. J. Cell Biol. 22:453-467.
44. Vaughan, S., B. Wickstead, K. Gull, and S. G. Addinall. 2004. Molecular evolution of FtsZ protein sequences encoded within the genomes of archaea, bacteria, and eukaryota. J. Mol. Evol. 58:19-29.
45. Weiss, D. S. 2004. Bacterial cell division and the septal ring. Mol. Microbiol. 54:588-597.
46. Zuber, B., I. Nikonenko, P. Klauser, D. Muller, and J. Dubochet. 2005. The mammalian central nervous synaptic cleft contains a high density of periodically organized complexes. Proc. Natl. Acad. Sci. USA 102:19192-19197.