The MreB-like protein Mbl of Streptomyces coelicolor A3(2) depends on MreB for proper localization and contributes to spore wall synthesis

Journal of Bacteriology

Volumn 193, Issue 7, 2011, Pages 1533-1542

  Heichlinger, Andrea ^a   Ammelburg, Moritz ^b   Kleinschnitz, Eva Maria ^a   Latus, Annette ^a   Maldener, Iris ^a   Flärdh, Klas ^c   Wohlleben, Wolfgang ^a   Muth, Günther ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; COMPLEMENTARY DNA; ENHANCED GREEN FLUORESCENT PROTEIN; MBL PROTEIN; MREB PROTEIN; RNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SPORE; BACTERIUM MUTANT; ESCHERICHIA COLI; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPOROGENESIS; STREPTOMYCES COELICOLOR; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; PROTEIN TRANSPORT; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR;

STREPTOMYCES COELICOLOR;

EID: 79951809110     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01100-10     Document Type: Article

References (52)

1. Alyahya, S. A., et al. 2009. RodZ, a component of the bacterial core morphogenic apparatus. Proc. Natl. Acad. Sci. U. S. A. 106:1239-1244.
2. Bennett, J. A., et al. 2009. Medium-dependent phenotypes of Streptomyces coelicolor with mutations in ftsI or ftsW. J. Bacteriol. 191:661-664.
3. Berman, H. M., et al. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242. (Pubitemid 30047768)
4. Bork, P., C. Sander, and A. Valencia. 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.
5. Bullock, W. O., J. M. Fernandez, and M. J. Short. 1987. X-L1blue, a high efficiency plasmid transforming recA Escherichia coli strain with beta galactosidase selection. Biotechniques 5:376-378.
6. Burger, A., K. Sichler, G. Kelemen, M. Buttner, and W. Wohlleben. 2000. Identification and characterization of the mre gene region of Streptomyces coelicolor A3(2). Mol. Gen. Genet. 263:1053-1060.
7. Carballido-López, R. 2006. The bacterial actin-like cytoskeleton. Microbiol. Mol. Biol. Rev. 70:888-909.
8. Carballido-López, R., et al. 2006. Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev. Cell 11:399-409. (Pubitemid 44283948)
9. Cherepanov, P. P., and W. Wackernagel. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
10. 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. (Pubitemid 36724940)
11. Defeu Soufo, H. J., and P. L. Graumann. 2004. Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep. 5:789-794.
12. Defeu Soufo, H. J., and P. L. Graumann. 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.
13. Defeu Soufo, H. J., et al. 2010. Bacterial translation elongation factor EF-Tu interacts and colocalizes with actin-like MreB protein. Proc. Natl. Acad. Sci. U. S. A. 107:3163-3168.
14. Divakaruni, A. V., C. Baida, C. L. White, and J. W. Gober. 2007. The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol. Microbiol. 66:174-188.
15. Dye, N. A., Z. Pincus, J. A. Theriot, L. Shapiro, and Z. Gitai. 2005. Two independent spiral structures control cell shape in Caulobacter. Proc. Natl. Acad. Sci. U. S. A. 102:18608-18613. (Pubitemid 43011273)
16. Errington, J. 2003. Dynamic proteins and a cytoskeleton in bacteria. Nat. Cell Biol. 5:175-178.
17. Figge, R. M., A. V. Divakaruni, and J. W. Gober. 2004. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51:1321-1332.
18. Formstone, A., and J. Errington. 2005. A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis. Mol. Microbiol. Mar;. 55:1646-1657. (Pubitemid 40445203)
19. Gerdes, K. 2009. RodZ, a new player in bacterial cell morphogenesis. EMBO J. 28:171-172.
20. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-Pdb- Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
21. Gust, B., G. L. Challis, K. Fowler, T. Kieser, and K. F. Chater. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. U. S. A. 100:1541-1546.
22. Hempel, A. M., S. B. Wang, M. Letek, J. A. Gil, and K. Flardh. 2008. Assemblies of DivIVA mark sites for hyphal branching and can establish new zones of cell wall growth in Streptomyces coelicolor. J. Bacteriol. 190:7579-7583.
23. Hong, H. J., M. S. Paget, and M. J. Buttner. 2002. A signal transduction system in Streptomyces coelicolor that activates the expression of a putative cell wall glycan operon in response to vancomycin and other cell wall-specific antibiotics. Mol. Microbiol. 44:1199-1211.
24. Hutchings, M. I., H. J. Hong, E. Leibovitz, I. C. Sutcliffe, and M. J. Buttner. 2006. The sigma(E) cell envelope stress response of Streptomyces coelicolor is influenced by a novel lipoprotein, CseA. J. Bacteriol. 188:7222-7229.
25. Jones, L. J., R. Carballido-Lopez, and J. Errington. 2001. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913-922. (Pubitemid 32289283)
26. Karimova, G., J. Pidoux, A. Ullmann, and D. Ladant. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U. S. A. 95:5752-5756.
27. Kawai, Y., K. Asai, and J. Errington. 2009. Partial functional redundancy of MreB isoforms, MreB, Mbl and MreBH, in cell morphogenesis of Bacillus subtilis. Mol. Microbiol. 73:719-731.
28. Kawai, Y., R. A. Daniel, and J. Errington. 2009. Regulation of cell wall morphogenesis in Bacillus subtilis by recruitment of PBP1 to the MreB helix. Mol. Microbiol. 71:1131-1144.
29. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, CT.
30. Kim, S. Y., Z. Gitai, A. Kinkhabwala, L. Shapiro, and W. E. Moerner. 2006. Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc. Natl. Acad. Sci. U. S. A. 103:10929-10934.
31. Kleinschnitz, E.-M., A. Heichlinger, K. Schirner, J. Winkler, A. Latus, I. Maldener, W. Wohlleben, and G. Muth. 18 January 2011. Proteins encoded by the mre gene cluster in Streptomyces coelicolor A3(2) cooperate in spore wall synthesis. Mol. Micorbiol. doi:10.1111/j.1365-2958.2010.07529.x. [Epub ahead of print.]
32. Kruse, T., et al. 2006. Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev. 20:113-124. (Pubitemid 43042672)
33. Kruse, T., J. Bork-Jensen, and K. Gerdes. 2005. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol. Microbiol. 55:78-89.
34. Kruse, T., and K. Gerdes. 2005. Bacterial DNA segregation by the actin-like MreB protein. Trends Cell Biol. 15:343-345. (Pubitemid 40943521)
35. Kruse, T., J. Moller-Jensen, A. Lobner-Olesen, and K. Gerdes. 2003. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J. 22:5283-5292. (Pubitemid 37222047)
36. Letek, M., et al. 2008. DivIVA is required for polar growth in the MreBlacking rod-shaped actinomycete Corynebacterium glutamicum. J. Bacteriol. 190:3283-3292. (Pubitemid 351581424)
37. MacNeil, D. J., et al. 1992. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111:61-68.
38. Mazza, P., et al. 2006. MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Mol. Microbiol. 60:838-852.
39. Nieselt, K., et al. 2010. The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics 11:10.
40. Paget, M. S., L. Chamberlin, A. Atrih, S. J. Foster, and M. J. Buttner. 1999. Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 181:204-211.
41. Pridmore, R. D. 1987. New and versatile cloning vectors with kanamycin-resistance marker. Gene 56:309-312. (Pubitemid 17152064)
42. Redenbach, M., et al. 1996. A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol. Microbiol. 21:77-96.
43. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
44. Sambrook, J., and D. W. Russel. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, NY.
45. Schirner, K., and J. Errington. 2009. Influence of heterologous MreB proteins on cell morphology of Bacillus subtilis. Microbiology 155:3611-3621.
46. Söding, J., A. Biegert, and A. N. Lupas. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33:W244-W248.
47. Tiffert, Y., et al. 2008. The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol. Microbiol. 67:861-880.
48. Tiyanont, K., et al. 2006. Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. Proc. Natl. Acad. Sci. U. S. A. 103:11033-11038.
49. van den Ent, F., L. A. Amos, and J. Lowe. 2001. Prokaryotic origin of the actin cytoskeleton. Nature 413:39-44. (Pubitemid 32843480)
50. van den Ent, F., C. M. Johnson, L. Persons, P. de Boer, and J. Lowe. 2010. Bacterial actin MreB assembles in complex with cell shape protein RodZ. EMBO J. 29:1081-1090.
51. van den Ent, F., J. Moller-Jensen, L. A. Amos, K. Gerdes, and J. Lowe. 2002. F-actin-like filaments formed by plasmid segregation protein ParM. EMBO J. 21:6935-6943. (Pubitemid 36014565)
52. Vollmer, W., and S. J. Seligman. 2010. Architecture of peptidoglycan: more data and more models. Trends Microbiol. 18:59-66.