Characterization of the Bacillus subtilis spore morphogenetic coat protein CotO

Journal of Bacteriology

Volumn 187, Issue 24, 2005, Pages 8278-8290

  McPherson, D C ^a   Kim, H ^a   Hahn, M ^a   Wang, R ^b   Grabowski, P ^c   Eichenberger, P ^c   Driks, A ^a  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b Illinois Institute of Technology   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COAT PROTEIN; COTO PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL SPORE; CELLULAR DISTRIBUTION; ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; SPOROGENESIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; GENE DELETION; GREEN FLUORESCENT PROTEINS; MACROMOLECULAR SUBSTANCES; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MORPHOGENESIS; MUTAGENESIS, INSERTIONAL; SPORES, BACTERIAL;

BACILLUS (BACTERIUM); BACILLUS ANTHRACIS; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 28844478962     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.24.8278-8290.2005     Document Type: Article

References (72)

1. Aronson, A. I., and P. Fitz-James. 1976. Structure and morphogenesis of the bacterial spore coat. Bacteriol. Rev. 40:360-402 .
2. Baccigalupi, L., G. Castaldo, G. Cangiano, R. Isticato, R. Marasco, M. De Felice, and E. Ricca. 2004. GerE-independent expression of cotH leads to CotC accumulation in the mother cell compartment during Bacillus subtilis sporulation. Microbiology 150:3441-3449.
3. Bagyan, I., J. Hobot, and S. Cutting. 1996. A compartmentalized regulator of developmental gene expression in Bacillus subtilis. J. Bacteriol. 178:4500-4507.
4. Bauer, T., S. Little, A. G. Stöver, and A. Driks. 1999. Functional regions of the B. subtilis spore coat morphogenetic protein CotE. J. Bacteriol. 181:7043-7051.
5. Beall, B., A. Driks, R. Losick, and C. P. Moran, Jr. 1993. Cloning and characterization of a gene required for assembly of the Bacillus subtilis spore coat. J. Bacteriol. 175:1705-1716.
6. Catalano, F. A., J. Meador-Parton, D. L. Popham, and A. Driks. 2001. Amino acids in the Bacillus subtilis morphogenetic protein SpoIVA with roles in spore coal and cortex formation. J. Bacteriol. 183:1645-1654.
7. Chada, V. G., E. A. Sanstad, R. Wang, and A. Driks. 2003. Morphogenesis of Bacillus spore surfaces. J. Bacteriol. 185:6255-6261.
8. Cutting, S., V. Oke, A. Driks, R. Losick, S. Lu, and L. Kroos. 1990. A forespore checkpoint for mother cell gene expression during development in B. subtilis. Cell 62:239-250.
9. Cutting, S., S. Panzer, and R. Losick. 1989. Regulatory studies on the promoter for a gene governing synthesis and assembly of the spore coat in Bacillus subtilis. J. Mol. Biol. 207:393-404.
10. Cutting, S. M., and P. B. Vander Horn. 1990. Molecular biological methods for Bacillus. John Wiley & Sons Ltd., Chichester, United Kingdom.
11. Donovan, W., L. Zheng, K. Sandman, and R. Losick. 1987. Genes encoding spore coat polypeptides from Bacillus subtilis. J. Mol. Biol. 196:1-10.
12. Driks, A. 1999. The Bacillus subtilis spore coat. Microbiol. Mol. Biol. Rev. 63:1-20.
13. Driks, A. 2003. The dynamic spore. Proc. Natl. Acad. Sci. USA 100:3007-3009.
14. Driks, A. 2002. Proteins of the spore core and coat, p. 527-536. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives. American Society for Microbiology, Washington, D.C.
15. Driks, A. 2004. The spore surface. In E. Ricca, A. Henriques, and C. Cutting (ed.), Bacterial spore formers: probiotics and emerging applications. Horizon Biosciencc, Norfolk, United Kingdom.
16. Driks, A., S. Roels, B. Beall, C. P. J. Moran, and R. Losick. 1994. Subcellular localization of proteins involved in the assembly of the spore coat of Bacillus subtilis. Genes Dev. 8:234-244.
17. Driks, A., and P. Setlow. 2000. Morphogenesis and properties of the bacterial spore, p. 191-218. In Y. V. Brun and L. J. Shimkets (ed.), Prokaryotic development. American Society for Microbiology, Washington, D.C.
18. Due le, H., H. A. Hong, N. Fairweather, E. Ricca, and S. M. Cutting. 2003. Bacterial spores as vaccine vehicles. Infect. Immun. 71:2810-2818.
19. Eichenberger, P., M. Fujita, S. T. Jensen, E. M. Conlon, D. Z. Rudner, S. T. Wang, C. Ferguson, K. Haga, T. Sato, J. S. Liu, and R. Losick. 2004. The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol. 2:e328.
20. Eichenberger, P., S. T. Jensen, E. M. Conlon, C. van Ooij, J. Silvaggi, J. E. Gonzalez-Pastor, M. Fujita, S. Ben-Yehuda, P. Stragier, J. S. Liu, and R. Losick. 2003. The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis. J. Mol. Biol. 327:945-972.
21. Feucht, A., L. Evans, and J. Errington. 2003. Identification of sporulation genes by genome-wide analysis of the sigmaE regulon of Bacillus subtilis. Microbiology 149:3023-3034.
22. Gadde, S., and R. Heald. 2004. Mechanisms and molecules of the mitotic spindle. Curr. Biol. 14:R797-R805.
23. Guerout-Fleury, A. M., N. Frandsen, and P. Stragier. 1996. Plasmids for ectopic integration in Bacillus subtilis. Gene 180:57-61.
24. Henriques, A. O., B. W. Beall, and C. P. J. Moran. 1997. CotM of Bacillus subtilis, a member of the alpha-crystallin family of stress proteins, is induced during development and participates in spore outer coat formation. J. Bacteriol. 179:1887-1897.
25. Henriques, A. O., T. V. Costa, L. O. Martins, and R. Zilhao. 2004. The functional architecture and assembly of the coat, p. 65-86. In R. E. Ricca, A. O. Henriques, and S. M. Cutting (ed.), Bacterial spore formers: probiotics and emerging applications. Horizon Biosciences, Norfolk, United Kingdom.
26. Henriques, A. O., L. R. Melsen, and C. P. Moran, Jr. 1998. Involvement of superoxide dismutase in spore coat assembly in Bacillus subtilis. J. Bacteriol. 180:2285-2291.
27. Henriques, A. O., and C. P. Moran, Jr. 2000. Structure and assembly of the bacterial endospore coat. Merthods 20:95-110.
28. Hilbert, D. W., and P. J. Piggot. 2004. Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol. Mol. Biol. Rev. 68:234-262.
29. Ireton, K., and A. Grossman. 1992. Interactions among mutations that cause altered timing of gene expression during sporulation in Bacillus subtilis. J. Bacteriol. 174:3185-3195.
30. Isticato, R., G. Esposito, R. Zilhao, S. Nolasco, G. Cangiano, M. De Felice, A. O. Henriques, and E. Ricca. 2004. Assembly of multiple CotC forms into the Bacillus subtilis spore coat. J. Bacteriol. 186:1129-1135.
31. Karmazyn-Campelli, C., L. Fluss, T. Leighton, and P. Stragier. 1992. The spoIIN279(ts) mutation affects the FtsA protein of Bacillus subtilis. Biochimie 74:689-694.
32. 31a. Kim, H., M. Hahn, P. Grabowski, D. McPherson, R. Wang, C. Ferguson, P. Eichenberger, and A. Driks. 2005. The Bacillus subtilis spore coat protein interaction network. Mol. Microbiol., in press.
33. Kim, H. S., D. Sherman, F. Johnson, and A. I. Aronson. 2004. Characterization of a major Bacillus anthracis spore coat protein and its role in spore inactivation. J. Bacteriol. 186:2413-2417.
34. Kuwana, R., Y. Kasahara, M. Fujibayashi, H. Takamatsu, N. Ogasawara, and K. Watabe. 2002. Proteomics characterization of novel spore proteins of Bacillus subtilis. Microbiology 148:3971-3982.
35. Lai, E.-M., N. D. Phadke, M. T. Kachman, R. Giorno, V. S. 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.
36. LeDeaux, J. R., and A. D. Grossman. 1995. Isolation and characterization of kinC, a gene lhat encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis. J. Bacteriol. 177:166-175.
37. Leiman, P. G., S. Kanamaru, V. Mesyanzhinov, F. Arisaka, and M. G. Rossmann. 2003. Structure and morphogenesis of bacteriophage T4. Cell Mol. Life Sci. 60:2356-2370.
38. Lemon, K. P., and A. D. Grossman. 1998. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282:1516-1519.
39. Little, S., and A. Driks. 2001. Functional analysis of the Bacillus subtilis morphogenetic spore coat protein CotE. Mol. Microbiol. 42:1107-1120.
40. Macnab, R. M. 2004. Type III flagellar protein export and flagellar assembly. Biochim. Biophys. Acta 1694:207-217.
41. Moir, A. 1981. Germination properties of a spore coat-defective mutant of Bacillus subtilis. J. Bacteriol. 146:1106-1116.
42. Naclerio, G., L. Baccigalupi, R. Zilhao, M. De Felice, and E. Ricca. 1996. Bacillus subtilis spore coat assembly requires cotH gene expression. J. Bacteriol. 178:4375-4380.
43. Nicholson, W. L. 2002. Roles of Bacillus endospores in the environment. Cell Mol. Life Sci. 59:410-416.
44. Nicholson, W. L., N. Munakata, G. Horneck, H. J. Melosh, and P. Setlow. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64:548-572.
45. Ozin, A. J., A. O. Henriques, H. Yi, and C. P. Moran, Jr. 2000. Morphogenetic proteins SpoVID and SafA form a complex during assembly of the Bacillus subtilis spore coat. J. Bacteriol. 182:1828-1833.
46. Ozin, A. J., C. S. Samford, A. O. Henriques, and C. P. Moran, Jr. 2001. SpoVID guides SafA to the spore coat in Bacillus subtilis. J. Bacteriol. 183:3041-3049.
47. Piggot, P. J., and J. G. Coote. 1976. Genetic aspects of bacterial endospore formation. Bacteriol. Rev. 40:908-962.
48. Plomp, M., T. Leighton, K. E. Wheeler, and A. J. Malkin. 2004. The high-resolution architecture and structural dynamics of Bacillus spores. Biophys. J. 88:603-608.
49. Pogliano, J., N. Osborne, M. D. Sharp, A. Abanes-De Mello, A. Perez, Y. L. Sun, and K. Pogliano. 1999. A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol. Microbiol. 31:1149-1159.
50. Pogliano, K., E. Harry, and R. Losick. 1995. Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol. Microbiol. 18:459-470.
51. Price, K. D., and R. Losick. 1999. A four-dimensional view of assembly of a morphogenetic protein during sporulation in Bacillus subtilis. J. Bacteriol. 181:781-790.
52. Ragkousi, K., and P. Setlow. 2004. Transglutaminase-mediated cross-linking of GerQ in the coats of Bacillus subtilis spores. J. Bacteriol. 186:5567-5575.
53. Roels, S., A. Driks, and R. Losick. 1992. Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis. J. Bacteriol. 174:575-585.
54. Sacco, M., E. Ricca, R. Losick, and S. Cutting. 1995. An additional GerE-controlled gene encoding an abundant spore coat protein from Bacillus subtilis. J. Bacteriol. 177:372-377.
55. Sauer, F. G., H. Remaut, S. J. Hultgren, and G. Waksman. 2004. Fiber assembly by the chaperone-usher pathway. Biochim. Biophys. Acta 1694:259-267.
56. Setlow, P. 2003. Spore germination. Curr. Opin. Microbiol. 6:550-556.
57. Sonenshein, A. L., J. A. Hoch, and R. Losick. 2002. Bacillus subtilis and its closest relatives. American Society for Microbiology, Washington, D.C.
58. Steil, L., M. Serrano, A. O. Henriques, and U. Volker. 2005. Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis. Microbiology 151:399-420.
59. Stevens, C. M., R. Daniel, N. Illing, and J. Errington. 1992. Characterization of a sporulation gene spoIVA involved in spore coat morphogenesis in Bacillus subtilis. J. Bacteriol. 174:586-594.
60. K and GerE during development and is located in the inner coat layer of spores. J. Bacteriol. 180:2968-2974.
61. Takamatsu, H., T. Kodama, T. Nakayama, and K. Watabe. 1999. Characterization of the yrbA gene of Bacillus subtilis, involved in resistance and germination of spores. J. Bacteriol. 181:4986-4994.
62. Takamatsu, H., T. Kodama, and K. Watabe. 1999. Assembly of the CotSA coat protein into spores requires CotS in Bacillus subtilis. FEMS Microbiol. Lett. 174:201-206.
63. van Ooij, C., P. Eichenberger, and R. Losick. 2004. Dynamic patterns of subcellular protein localization during spore coat morphogenesis in Bacillus subtilis. J. Bacteriol. 186:4441-4448.
64. Warth, A. D., D. F. Ohye, and W. G. Murrell. 1963. The composition and structure of bacterial spores. J. Cell Biol. 16:579-592.
65. Webb, C. D., A. Decatur, A. Teleman, and R. Losick. 1995. Use of green fluorescent protein for visualization of cell-specific gene expression and subcellular protein localization during sporulation in Bacillus subtilis. J. Bacteriol. 177:5906-5911.
66. Westphal, A. J., P. B. Price, T. J. Leighton, and K. E. Wheeler. 2003. Kinetics of size changes of individual Bacillus thuringiensis spores in response to changes in relative humidity. Proc. Natl. Acad. Sci. USA 100:3461-3466.
67. Youngman, P., J. B. Perkins, and R. Losick. 1984. Construction of a cloning site near one end of Tn917 into which foreign DNA may be inserted without affecting transposition in Bacillus subtilis or expression of the transposonborne erm gene. Plasmid 12:1-9.
68. Zhang, J., P. C. Fitz-James, and A. I. Aronson. 1993. Cloning and characterization of a cluster of genes encoding polypeptides present in the insoluble fraction of the spore coat of Bacillus subtilis. J. Bacteriol. 175:3757-3766.
69. Zheng, L., W. P. Donovan, P. C. Fitz-James, and R. Losick. 1988. Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Genes Dev. 2:1047-1054.
70. Zheng, L., and R. Losick. 1990. Cascade regulation of spore coat gene expression in Bacillus subtilis. J. Mol. Biol. 212:645-660.
71. Zilhao, R., G. Naclerio, A. O. Henriques, L. Baccigalupi, C. P. Moran, Jr., and E. Ricca. 1999. Assembly requirements and role of CotH during spore coat formation in Bacillus subtilis. J. Bacteriol. 181:2631-2633.
72. Zilhao, R., M. Serrano, R. Isticato, E. Ricca, C. P. Moran, Jr., and A. O. Henriques. 2004. Interactions among CotB, CotG, and CotH during assembly of the Bacillus subtilis spore coat. J. Bacteriol. 186:1110-1119.