Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor

Journal of Bacteriology

Volumn 191, Issue 21, 2009, Pages 6501-6512

  Haiser, Henry J ^a   Yousef, Mary R ^a   Elliot, Marie A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROLASE; PROTEIN RPFA; PROTEIN SW 1 A; PROTEIN SW 1 B; PROTEN SW 1 C; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; CELL DIFFERENTIATION; CELL WALL; COMPUTER MODEL; CONTROLLED STUDY; FUNGUS HYPHAE; GENE DELETION; LIFE CYCLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SPORE GERMINATION; SPOROGENESIS; STREPTOMYCES COELICOLOR; UNTRANSLATED REGION; VEGETATIVE GROWTH;

BASE SEQUENCE; CELL WALL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYDROLASES; MOLECULAR SEQUENCE DATA; MUTATION; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOMYCES COELICOLOR;

EID: 70350440341     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00767-09     Document Type: Article

References (56)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Meyers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Anantharaman, V., and L. Aravind. 2003. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 4:R11.
3. Barreteau, H., A. Kovac, A. Boniface, M. Sova, S. Gobec, and D. Blanot. 2008. Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol. Rev. 32:168-207.
4. Barrick, J. E., K. A. Corbino, W. C. Winkler, A. Nahvi, M. Mandal, J. Collins, M. Lee, A. Roth, N. Sudarsan, I. Jona, J. K. Wickiser, and R. R. Breaker. 2004. New RNA motifs suggest an expanded scope for riboswitches in bacterial genetic control. Proc. Natl. Acad. Sci. USA 101:6421-6426.
5. Bateman, A., E. Birney, R. Durbin, S. R. Eddy, K. L. Howe, and E. L. Sonnhammer. 2000. The Pfam protein families database. Nucleic Acids Res. 28:263-266.
6. Bendtsen, J. D., H. Nielsen, H. G. von, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
7. Bentley, S. D., K. F. Chater, A. M. Cerdeno-Tárraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147.
8. Bouhss, A., A. E. Trunkfield, T. D. Bugg, and D. Mengin-Lecreulx. 2008. The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol. Rev. 32:208-233.
9. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Buist, G., A. Steen, J. Kok, and O. P. Kuipers. 2008. LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68:838-847.
11. Carballido-López, R., A. Formstone, Y. Li, S. D. Ehrlich, P. Noirot, and J. Errington. 2006. Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev. Cell 11:399-409. (Pubitemid 44283948)
12. Cohen-Gonsaud, M., N. H. Keep, A. P. Davies, J. Ward, B. Henderson, and G. Labesse. 2004. Resuscitation-promoting factors possess a lysozyme-like domain. Trends Biochem. Sci. 29:7-10.
13. Cohen-Gonsaud, M., P. Barthe, C. Bagneris, B. Henderson, J. Ward, C. Roumestand, and N. H. Keep. 2005. The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes. Nat. Struct. Mol. Biol. 12:270-273.
14. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
15. Derouaux, A., S. Halici, H. Nothaft, T. Neutelings, G. Moutzourelis, J. Dusart, F. Titgemeyer, and S. Rigali. 2004. Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. J. Bacteriol. 186:1893-1897. (Pubitemid 38314535)
16. Dramsi, S., S. Magnet, S. Davison, and M. Arthur. 2008. Covalent attachment of proteins to peptidoglycan. FEMS Microbiol. Rev. 32:307-320.
17. Elliot, M. A., N. Karoonuthaisiri, J. Huang, M. J. Bibb, S. N. Cohen, C. M. Kao, and M. J. Buttner. 2003. The chaplins: a family of hydrophobic cellsurface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev. 17:1727-1740. (Pubitemid 36870336)
18. Engel, H., B. Kazemier, and W. Keck. 1991. Murein-metabolizing enzymes from Escherichia coli: sequence analysis and controlled overexpression of the slt gene, which encodes the soluble lytic transglycosylase. J. Bacteriol. 173:6773-6782.
19. Firczuk, M., and M. Bochtler. 2007. Folds and activities of peptidoglycan amidases. FEMS Microbiol. Rev. 31:676-691.
20. 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. USA 100:1541-1546.
21. Haiser, H. J., F. V. Karginov, G. J. Hannon, and M. A. Elliot. 2008. Developmentally regulated cleavage of tRNAs in the bacterium Streptomyces coelicolor. Nucleic Acids Res. 36:732-741.
22. Hempel, A. M., S. B. Wang, M. Letek, J. A. Gil, and K. Flärdh. 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. Hett, E. C., M. C. Chao, A. J. Steyn, S. M. Fortune, L. L. Deng, and E. J. Rubin. 2007. A partner for the resuscitation-promoting factors of Mycobacterium tuberculosis. Mol. Microbiol. 66:658-668.
24. Holtje, J. V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.
25. Janssen, G. R., and M. J. Bibb. 1993. Derivatives of pUC18 that have BglII sites flanking a modified multiple cloning site and that retain the ability to identify recombinant clones by visual screening of Escherichia coli colonies. Gene 124:133-134. (Pubitemid 23065980)
26. Kana, B. D., B. G. Gordhan, K. J. Downing, N. Sung, G. Vostroktunova, E. E. Machowski, L. Tsenova, M. Young, A. Kaprelyants, G. Kaplan, and V. Mizrahi. 2008. The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol. Microbiol. 67:672-684.
27. 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. USA 95:5752-5756.
28. Kieser, T., M. Bibb, M. Buttner, K. Chater, and D. Hopwood. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, United Kingdom.
29. Korat, B., H. Mottl, and W. Keck. 1991. 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.
30. Kuroda, A., and J. Sekiguchi. 1990. Cloning, sequencing and genetic mapping of a Bacillus subtilis cell wall hydrolase gene. J. Gen. Microbiol. 136:2209-2216.
31. LeClerc, D., and A. Asselin. 1989. Detection of bacterial cell wall hydrolases after denaturing polyacrylamide gel electrophoresis. Can. J. Microbiol. 35:749-753.
32. MacNeil, D. J., K. M. Gewain, C. L. Ruby, G. Dezeny, P. H. Gibbons, and T. MacNeil. 1992. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111:61-68.
33. Margot, P., M. Wahlen, A. Gholamhoseinian, P. Piggot, and D. Karamata. 1998. The lytE gene of Bacillus subtilis 168 encodes a cell wall hydrolase. J. Bacteriol. 180:749-752.
34. Mazza, P., E. E. Noens, K. Schirner, N. Grantcharova, A. M. Mommaas, H. K. Koerten, G. Muth, K. Flärdh, G. P. van Wezel, and W. Wohlleben. 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.
35. Molle, V., W. J. Palframan, K. C. Findlay, and M. J. Buttner. 2000. WhiD and WhiB, homologous proteins required for different stages of sporulation in Streptomyces coelicolor A3(2). J. Bacteriol. 182:1286-1295.
36. Mukamolova, G. V., O. A. Turapov, K. Kazarian, M. Telkov, A. S. Kaprelyants, D. B. Kell, and M. Young. 2002. The rpf gene of Micrococcus luteus encodes an essential secreted growth factor. Mol. Microbiol. 46:611-621.
37. Mukamolova, G. V., A. S. Kaprelyants, D. I. Young, M. Young, and D. B. Kell. 1998. A bacterial cytokine. Proc. Natl. Acad. Sci. USA 95:8916-8921.
38. Mukamolova, G. V., A. G. Murzin, E. G. Salina, G. R. Demina, D. B. Kell, A. S. Kaprelyants, and M. Young. 2006. Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol. Microbiol. 59:84-98.
39. Mukamolova, G. V., O. A. Turapov, D. I. Young, A. S. Kaprelyants, D. B. Kell, and M. Young. 2002. A family of autocrine growth factors in Mycobacterium tuberculosis. Mol. Microbiol. 46:623-635.
40. Noens, E. E., V. Mersinias, B. A. Traag, C. P. Smith, H. K. Koerten, and G. P. van Wezel. 2005. SsgA-like proteins determine the fate of peptidoglycan during sporulation of Streptomyces coelicolor. Mol. Microbiol. 58:929-944.
41. Nudler, E., and A. S. Mironov. 2004. The riboswitch control of bacterial metabolism. Trends Biochem. Sci. 29:11-17.
42. E is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 181:204-211.
43. Piette, A., A. Derouaux, P. Gerkens, E. E. E. Noens, G. Mazzucchelli, S. Vion, H. K. Koerten, F. Titgemeyer, E. De Pauw, P. Leprince, G. P. van Wezel, M. Galleni, and S. Rigali. 2005. From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant. J. Proteome Res. 4:1699-1708. (Pubitemid 41464797)
44. Ravagnani, A., C. L. Finan, and M. Young. 2005. A novel firmicute protein family related to the actinobacterial resuscitation-promoting factors by nonorthologous domain displacement. BMC Genomics 6:39. (Pubitemid 41357696)
45. Romeo, T. 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol. Microbiol. 29:1321-1330.
46. Roth, A., W. C. Winkler, E. E. Regulski, B. W. K. Lee, J. Lim, I. Jona, J. E. Barrick, A. Ritwik, J. N. Kim, R. Welz, D. Iwata-Reuyl, and R. R. Breaker. 2007. A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat. Struct. Mol. Biol. 14:308-317.
47. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Sauvage, E., F. Kerff, M. Terrak, J. A. Ayala, and P. Charlier. 2008. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol. Rev. 32:234-258.
49. Schleifer, K. H., and O. Kandler. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Microbiol. Mol. Biol. Rev. 36:407-477.
50. Setlow, P. 2003. Spore germination. Curr. Opin. Microbiol. 6:550-556.
51. Smith, T. J., S. A. Blackman, and S. J. Foster. 2000. Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249-262.
52. Steen, A., G. Buist, N. E. Kramer, R. Jalving, G. F. J. D. Benus, G. Venema, O. P. Kuipers, and J. Kok. 2008. Reduced lysis upon growth of Lactococcus lactis on galactose is a consequence of decreased binding of the autolysin AcmA. Appl. Environ. Microbiol. 74:4671-4679.
53. Swiercz, J. P., Hindra, J. Bobek, H. J. Haiser, B. C. Di Berardo, B. Tjaden, and M. A. Elliot. 2008. Small non-coding RNAs in Streptomyces coelicolor. Nucleic Acids Res. 36:7240-7251.
54. Ursinus, A., and J. V. Holtje. 1994. Purification and properties of a membrane-bound lytic transglycosylase from Escherichia coli. J. Bacteriol. 176:338-343. (Pubitemid 24034050)
55. Vollmer, W., B. Joris, P. Charlier, and S. Foster. 2008. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32:259-286.
56. Winkler, W. C., A. Nahvi, A. Roth, J. A. Collins, and R. R. Breaker. 2004. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281-286. (Pubitemid 38418792)