Roles of Germination-Specific Lytic Enzymes CwlJ and SleB in Bacillus anthracis

Journal of Bacteriology

Volumn 191, Issue 7, 2009, Pages 2237-2247

  Heffron, Jared D ^a   Orsburn, Benjamin ^a   Popham, David L ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; CWLJ1 PROTEIN; CWLJ2 PROTEIN; GENE PRODUCT; GLYCOSYLTRANSFERASE; MUROPEPTIDE; PEPTIDOGLYCAN; SLEB PROTEIN; UNCLASSIFIED DRUG; AMIDASE; HYDROLASE; SLEB PROTEIN, BACILLUS;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIUM COLONY; BACTERIUM MUTANT; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; HYDROLYSIS; NONHUMAN; NULL ALLELE; OPTICAL DENSITY; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SPORE GERMINATION; SPOROGENESIS; WILD TYPE; BACTERIAL SPORE; CELL WALL; CHEMISTRY; ENZYMOLOGY; GENETICS; MASS SPECTROMETRY; METABOLISM; PHYSIOLOGY;

BACILLI (CLASS); BACILLUS ANTHRACIS;

AMIDOHYDROLASES; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; CELL WALL; HYDROLASES; HYDROLYSIS; MASS SPECTROMETRY; SPORES, BACTERIAL;

EID: 64049117377     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01598-08     Document Type: Article

References (44)

1. Atrih, A., and S. J. Foster. 2001. In vivo roles of the germination-specific lytic enzymes of Bacillus subtilis 168. Microbiology 147:2925-2932.
2. Atrih, A., P. Zollner, G. Allmaier, M. P. Williamson, and S. J. Foster. 1998. Peptidoglycan structural dynamics during germination of Bacillus subtilis 168 endospores. J. Bacteriol. 180:4603-4612.
3. Bagyan, I., and P. Setlow. 2002. Localization of the cortex lytic enzyme CwlJ in spores of Bacillus subtilis. J. Bacteriol. 184:1219-1224.
4. Bergman, N. H., E. C. Anderson, E. E. Swenson, M. M. Niemeyer, A. D. Miyoshi, and P. C. Hanna. 2006. Transcriptional profiling of the Bacillus anthracis life cycle in vitro and an implied model for regulation of spore formation. J. Bacteriol. 188:6092-6100.
5. Boland, F. M., A. Atrih, H. Chirakkal, S. J. Foster, and A. Moir. 2000. Complete spore-cortex hydrolysis during germination of Bacillus subtilis 168 requires SleB and YpeB. Microbiology 146:57-64.
6. Chen, Y., S. Fukuoka, and S. Makino. 2000. A novel spore peptidoglycan hydrolase of Bacillus cereus: biochemical characterization and nucleotide sequence of the corresponding gene, sleL. J. Bacteriol. 182:1499-1506.
7. Chen, Y., S. Miyata, S. Makino, and R. Moriyama. 1997. Molecular characterization of a germination-specific muramidase from Clostridium perfringens S40 spores and nucleotide sequence of the corresponding gene. J. Bacteriol. 179:3181-3187.
8. Chirakkal, H., M. O'Rourke, A. Atrih, S. J. Foster, and A. Moir. 2002. Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination. Microbiology 148:2383-2392.
9. Cowan, A. E., D. E. Koppel, B. Setlow, and P. Setlow. 2003. A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: implications for spore dormancy. Proc. Natl. Acad. Sci. USA 100: 4209-4214.
10. Dowd, M. M., B. Orsburn, and D. L. Popham. 2008. Cortex peptidoglycan lytic activity in germinating Bacillus anthracis spores. J. Bacteriol. 190:4541- 4548.
11. Fisher, N., and P. Hanna. 2005. Characterization of Bacillus anthracis germinant receptors in vitro. J. Bacteriol. 187:8055-8062.
12. Hanna, P. C., and J. A. Ireland. 1999. Understanding Bacillus anthracis pathogenesis. Trends Microbiol. 7:180-182.
13. Helmann, J. D., and C. P. Moran, Jr. 2001. RNA polymerase and sigma factors, p. 289-312. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its close relatives: from genes to cells. American Society for Microbiology, Washington, DC.
14. Höltje, J. V., D. Mirelman, N. Sharon, and U. Schwarz. 1975. Novel type of murein transglycosylase in Escherichia coli. J. Bacteriol. 124:1067-1076.
15. Howell, A., S. Dubrac, K. K. Andersen, D. Noone, J. Fert, T. Msadek, and K. Devine. 2003. Genes controlled by the essential YycG/YycF two-component system of Bacillus subtilis revealed through a novel hybrid regulator approach. Mol. Microbiol. 49:1639-1655.
16. Ishikawa, S., K. Yamane, and J. Sekiguchi. 1998. Regulation and characterization of a newly deduced cell wall hydrolase gene (cwlJ) which affects germination of Bacillus subtilis spores. J. Bacteriol. 180:1375-1380.
17. Janes, B. K., and S. Stibitz. 2006. Routine markerless gene replacement in Bacillus anthracis. Infect. Immun. 74:1949-1953.
18. Kim, H. U., and J. M. Goepfert. 1974. A sporulation medium for Bacillus anthracis. J. Appl. Bacteriol. 37:265-267.
19. Lai, E. M., N. D. Phadke, M. T. Kachman, R. Giorno, S. Vazquez, J. A. Vazquez, J. R. Maddock, and A. Driks. 2003. Proteomic analysis of the spore coats of Bacillus subtilis and Bacillus anthracis. J. Bacteriol. 185:1443-1454.
20. Lambert, E. A., and D. L. Popham. 2008. The Bacillus anthracis SleL (YaaH) protein is an N-acetylglucosaminidase involved in spore cortex depolymerization. J. Bacteriol. 190:7601-7607.
21. Liu, H., N. H. Bergman, B. Thomason, S. Shallom, A. Hazen, J. Crossno, D. A. Rasko, J. Ravel, T. D. Read, S. N. Peterson, J. Yates III, and P. C. Hanna. 2004. Formation and composition of the Bacillus anthracis endospore. J. Bacteriol. 186:164-178.
22. Mäder, U., G. Homuth, C. Scharf, K. Büttner, R. Bode, and M. Hecker. 2002. Transcriptome and proteome analysis of Bacillus subtilis gene expression modulated by amino acid availability. J. Bacteriol. 184:4288-4295.
23. Magge, A., A. C. Granger, P. G. Wahome, B. Setlow, V. R. Vepachedu, C. A. Loshon, L. Peng, D. Chen, Y. Q. Li, and P. Setlow. 2008. Role of dipicolinic acid in the germination, stability, and viability of spores of Bacillus subtilis. J. Bacteriol. 190:4798-4807.
24. Makino, S., and R. Moriyama. 2002. Hydrolysis of cortex peptidoglycan during bacterial spore germination. Med. Sci. Monit. 8:RA119-RA127.
25. Masayama, A., H. Fukuoka, S. Kato, T. Yoshimura, M. Moriyama, and R. Moriyama. 2006. Subcellular localization of a germiantion-specific cortexlytic enzyme, SleB, of bacilli during sporulation. Genes Genet. Syst. 81:163- 169.
26. Meador-Parton, J., and D. L. Popham. 2000. Structural analysis of Bacillus subtilis spore peptidoglycan during sporulation. J. Bacteriol. 182:4491-4499.
27. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratories, Cold Spring Harbor, NY.
28. Miyata, S., R. Moriyama, N. Miyahara, and S. Makino. 1995. A gene (sleC) encoding a spore-cortex-lytic enzyme from Clostridium perfringens S40 spores; cloning, sequence analysis and molecular characterization. Microbiology 141:2643-2650.
29. Moir, A. 2006. How do spores germinate? J. Appl. Microbiol. 101:526-530.
30. Moir, A., B. M. Corfe, and J. Behravan. 2002. Spore germination. Cell. Mol. Life Sci. 59:403-409.
31. Morgulis, A., G. Coulouris, Y. Raytselis, T. L. Madden, R. Agarwala, and A. A. Schaffer. 2008. Database indexing for production MegaBLAST searches. Bioinformatics 24:1757-1764.
32. Moriyama, R., H. Fukuoka, S. Miyata, S. Kudoh, A. Hattori, S. Kozuka, Y. Yasuda, K. Tochikubo, and S. Makino. 1999. Expression of a germinationspecific amidase, SleB, of bacilli in the forespore compartment of sporulating cells and its localization on the exterior side of the cortex in dormant spores. J. Bacteriol. 181:2373-2378.
33. Moriyama, R., A. Hattori, S. Miyata, S. Kudoh, and S. Makino. 1996. A gene (sleB) encoding a spore cortex-lytic enzyme from Bacillus subtilis and response of the enzyme to L-alanine-mediated germination. J. Bacteriol. 178: 6059-6063.
34. Nicholson, W. L., and P. Setlow. 1990. Sporulation, germination, and outgrowth, p. 391-450. In C. R. Harwood and S. M. Cutting (ed.), Molecular biological methods for Bacillus. John Wiley & Sons, Ltd., Chichester, England.
35. Orsburn, B., S. B. Melville, and D. L. Popham. 2008. Factors contributing to heat resistance of Clostridium perfringens endospores. Appl. Environ. Microbiol. 74:3328-3335.
36. Paidhungat, M., K. Ragkousi, and P. Setlow. 2001. Genetic requirements for induction of germination of spores of Bacillus subtilis by Ca2-dipicolinate. J. Bacteriol. 183:4886-4893.
37. Popham, D. L., J. Helin, C. E. Costello, and P. Setlow. 1996. Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spore outgrowth but not for spore dehydration or heat resistance. Proc. Natl. Acad. Sci. USA 93:15405-15410.
38. Quinn, C. P., and B. N. Dancer. 1990. Transformation of vegetative cells of Bacillus anthracis with plasmid DNA. J. Gen. Microbiol. 136:1211-1215.
39. Ragkousi, K., P. Eichenberger, C. van Ooij, and P. Setlow. 2003. Identification of a new gene essential for germination of Bacillus subtilis spores with Ca2-dipicolinate. J. Bacteriol. 185:2315-2329.
40. Schleifer, K. H., and O. Kandler. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36:407-477.
41. Setlow, B., E. Melly, and P. Setlow. 2001. Properties of spores of Bacillus subtilis blocked at an intermediate stage in spore germination. J. Bacteriol. 183:4894-4899.
42. Setlow, P. 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101:514-525.
43. Warth, A. D., and J. L. Strominger. 1969. Structure of the peptidoglycan of bacterial spores: occurrence of the lactam of muramic acid. Proc. Natl. Acad. Sci. USA 64:528-535.
44. Zhang, Z., S. Schwartz, L. Wagner, and W. Miller. 2000. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7:203-214.