The coat morphogenetic protein SpoVID is necessary for spore encasement in Bacillus subtilis

Molecular Microbiology

Volumn 74, Issue 3, 2009, Pages 634-649

  Wang, Katherine H ^a   Isidro, Anabela L ^b   Domingues, Lia ^b   Eskandarian, Haig A ^a   McKenney, Peter T ^a   Drew, Kevin ^a,c   Grabowski, Paul ^a,d   Chua, Ming Hsiu ^a   Barry, Samantha N ^a   Guan, Michelle ^a   Bonneau, Richard ^a,c   Henriques, Adriano O ^b   Eichenberger, Patrick ^a  

^a NEW YORK UNIVERSITY   (United States)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c NEW YORK UNIVERSITY   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; PROTEIN SPOIVA; PROTEIN SPOVID; PROTEIN SPOVM; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL STRAIN; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

AMINO ACID SUBSTITUTION; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CONSERVED SEQUENCE; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GREEN FLUORESCENT PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MORPHOGENESIS; MUTATION; PEPTIDE LIBRARY; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; SPORES, BACTERIAL; TWO-HYBRID SYSTEM TECHNIQUES;

BACILLUS SUBTILIS;

EID: 70350432748     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06886.x     Document Type: Article

References (72)

1. Alber, F., Dokudovskaya, S., Veenhoff, L.M., Zhang, W., Kipper, J., Devos, D., et al. (2007) Determining the architectures of macromolecular assemblies. Nature 450 : 683 694.
2. Beall, B., Driks, A., Losick, R. Moran, C.P., Jr (1993) Cloning and characterization of a gene required for assembly of the Bacillus subtilis spore coat. J Bacteriol 175 : 1705 1716.
3. Bourne, N., FitzJames, P.C. Aronson, A.I. (1991) Structural and germination defects of Bacillus subtilis spores with altered contents of a spore coat protein. J Bacteriol 173 : 6618 6625.
4. Boydston, J.A., Yue, L., Kearney, J.F. Turnbough, C.L., Jr (2006) The ExsY protein is required for complete formation of the exosporium of Bacillus anthracis. J Bacteriol 188 : 7440 7448.
5. Buist, G., Steen, A., Kok, J. Kuipers, O.P. (2008) LysM, a widely distributed protein motif for binding to (peptido) glycans. Mol Microbiol 68 : 838 847.
6. Campanacci, V., Bishop, R.E., Blangy, S., Tegoni, M. Cambillau, C. (2006) The membrane bound bacterial lipocalin Blc is a functional dimer with binding preference for lysophospholipids. FEBS Lett 580 : 4877 4883.
7. Costa, T., Isidro, A.L., Moran, C.P. Henriques, A.O. (2006) Interaction between coat morphogenetic proteins SafA and SpoVID. J Bacteriol 188 : 7731 7741.
8. Cutting, S., Zheng, L.B. Losick, R. (1991) Gene encoding two alkali-soluble components of the spore coat from Bacillus subtilis. J Bacteriol 173 : 2915 2919.
9. Dokland, T., McKenna, R., Ilag, L.L., Bowman, B.R., Incardona, N.L., Fane, B.A. Rossmann, M.G. (1997) Structure of a viral procapsid with molecular scaffolding. Nature 389 : 308 313.
10. Donovan, W., Zheng, L.B., Sandman, K. Losick, R. (1987) Genes encoding spore coat polypeptides from Bacillus subtilis. J Mol Biol 196 : 1 10.
11. Driks, A. (1999) Bacillus subtilis spore coat. Microbiol Mol Biol Rev 63 : 1 20.
12. Driks, A. (2002a) Proteins of the spore core and coat. In Bacillus Subtilis and its Closest Relatives: from Genes to Cells. Sonenshein, A.L., Hoch, J.A Losick, R. (eds). Washington, DC : American Society for Microbiology, pp. 527 536.
13. Driks, A. (2002b) Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol 10 : 251 254.
14. Driks, A., Roels, S., Beall, B., Moran, C.P. Losick, R. (1994) Subcellular localization of proteins involved in the assembly of the spore coat of Bacillus subtilis. Genes Dev 8 : 234 244.
15. Eichenberger, P. (2007) Genomics and cellular biology of endospore formation. In Bacillus Cellular and Molecular Biology. Graumann, P. (ed.). Norfolk : Caister Academic Press, pp. 375 418.
16. Eichenberger, P., Jensen, S.T., Conlon, E.M., van Ooij, C., Silvaggi, J., Gonzalez-Pastor, J.E., et al. (2003) The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis. J Mol Biol 327 : 945 972.
17. Eichenberger, P., Fujita, M., Jensen, S.T., Conlon, E.M., Rudner, D.Z., Wang, S.T., et al. (2004) The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol 2 : e328.
18. Einarson, M.B. Orlinick, J.R. (2002) Identification of protein-protein interactions with gluthatione-S-transferase fusion proteins. In Protein-Protein Interactions. Golemis, E. (ed.). Cold Spring Harbor, NY : Cold Spring Harbor Laboratory Press, pp. 375 418.
19. Errington, J. (2003) Regulation of endospore formation in Bacillus subtilis. Nat Rev Microbiol 1 : 117 126.
20. Frand, A.R., Russel, S. Ruvkun, G. (2005) Functional genomic analysis of C. elegans molting. PLoS Biol 3 : e312.
21. Giorno, R., Mallozzi, M., Bozue, J., Moody, K.S., Slack, A., Qiu, D., et al. (2009) Localization and assembly of proteins comprising the outer structures of the Bacillus anthracis spore. Microbiology 155 : 1133 1145.
22. Goehring, N.W. Beckwith, J. (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15 : R514 R526.
23. Grzyb, J., Latowski, D. Strzalka, K. (2006) Lipocalins - a family portrait. J Plant Physiol 163 : 895 915.
24. Henriques, A.O. Moran, C.P., Jr (2007) Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 61 : 555 588.
25. Henriques, A.O., Beall, B.W., Roland, K. Moran, C.P., Jr (1995) Characterization of cotJ, a sigma E-controlled operon affecting the polypeptide composition of the coat of Bacillus subtilis spores. J Bacteriol 177 : 3394 3406.
26. Henriques, A.O., Beall, B.W. Moran, C.P., Jr. (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.
27. Henriques, A.O., Costa, T.V., Martins, L.O. Zilhao, R. (2004) The functional architecture and assembly of the spore coat. In Bacterial Spore Formers, Probiotics and Emerging Applications. Ricca, E., Henriques, A.O. Cutting, S.M. (eds). Norfolk : Horizon Bioscience, pp. 65 85.
28. Jaroszewski, L., Rychlewski, L., Li, Z., Li, W. Godzik, A. (2005) FFAS03: a server for profile - profile sequence alignments. Nucleic Acids Res 33 : W284 W288.
29. Kaksonen, M., Toret, C.P. Drubin, D.G. (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123 : 305 320.
30. Kim, H., Hahn, M., Grabowski, P., McPherson, D.C., Otte, M.M., Wang, R., et al. (2006) The Bacillus subtilis spore coat protein interaction network. Mol Microbiol 59 : 487 502.
31. Klobutcher, L.A., Ragkousi, K. Setlow, P. (2006) The Bacillus subtilis spore coat provides 'eat resistance' during phagocytic predation by the protozoan Tetrahymena thermophila. Proc Natl Acad Sci USA 103 : 165 170.
32. Kuwana, R., Kasahara, Y., Fujibayashi, M., Takamatsu, H., Ogasawara, N. Watabe, K. (2002) Proteomics characterization of novel spore proteins of Bacillus subtilis. Microbiology 148 : 3971 3982. (Pubitemid 36097459)
33. Laaberki, M.H. Dworkin, J. (2008) Role of spore coat proteins in the resistance of Bacillus subtilis spores to Caenorhabditis elegans predation. J Bacteriol 190 : 6197 6203.
34. Lai, E.M., Phadke, N.D., Kachman, M.T., Giorno, R., Vazquez, S., Vazquez, J.A., et al. (2003) Proteomic analysis of the spore coats of Bacillus subtilis and Bacillus anthracis. J Bacteriol 185 : 1443 1454.
35. Lambert, E.A. Popham, D.L. (2008) The Bacillus anthracis SleL (YaaH) protein is an N-acetylglucosaminidase involved in spore cortex depolymerization. J Bacteriol 190 : 7601 7607.
36. Levin, P.A., Fan, N., Ricca, E., Driks, A., Losick, R. Cutting, S. (1993) An unusually small gene required for sporulation by Bacillus subtilis. Mol Microbiol 9 : 761 771.
37. McCarter, L.L. (2006) Regulation of flagella. Curr Opin Microbiol 9 : 180 186.
38. McPherson, D.C., Kim, H., Hahn, M., Wang, R., Grabowski, P., Eichenberger, P. Driks, A. (2005) Characterization of the Bacillus subtilis spore morphogenetic coat protein CotO. J Bacteriol 187 : 8278 8290.
39. Masayama, A., Kuwana, R., Takamatsu, H., Hemmi, H., Yoshimura, T., Watabe, K. Moriyama, R. (2007) A novel lipolytic enzyme, YcsK (LipC), located in the spore coat of Bacillus subtilis, is involved in spore germination. J Bacteriol 189 : 2369 2375.
40. Naclerio, G., Baccigalupi, L., Zilhao, R., De Felice, M. Ricca, E. (1996) Bacillus subtilis spore coat assembly requires cotH gene expression. J Bacteriol 178 : 4375 4380.
41. Nicholson, W.L. (2003) Using thermal inactivation kinetics to calculate the probability of extreme spore longevity: implications for paleomicrobiology and lithopanspermia. Orig Life Evol Biosph 33 : 621 631.
42. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J. Setlow, P. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64 : 548 572.
43. van Ooij, C. Losick, R. (2003) Subcellular localization of a small sporulation protein in Bacillus subtilis. J Bacteriol 185 : 1391 1398.
44. van Ooij, C., Eichenberger, P. Losick, R. (2004) Dynamic patterns of subcellular protein localization during spore coat morphogenesis in Bacillus subtilis. J Bacteriol 186 : 4441 4448.
45. Ozin, A.J., Henriques, A.O., Yi, H. Moran, C.P., 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., Samford, C.S., Henriques, A.O. Moran, C.P., Jr (2001) SpoVID guides SafA to the spore coat in Bacillus subtilis. J Bacteriol 183 : 3041 3049.
47. Paredes, C.J., Alsaker, K.V. Papoutsakis, E.T. (2005) A comparative genomic view of clostridial sporulation and physiology. Nature Rev Microbiol 3 : 969 978.
48. Piggot, P.J. Coote, J.G. (1976) Genetic aspects of bacterial endospore formation. Bacteriol Rev 40 : 908 962.
49. Piggot, P.J. Losick, R. (2002) Sporulation genes and intercompartmental regulation. In Bacillus Subtilis and its Closest Relatives: from Genes to Cells. Sonenshein, A.L., Hoch, J.A. Losick, R. (eds). Washington, DC : American Society for Microbiology, pp. 483 518.
50. Pogliano, J., Osborne, N., Sharp, M.D., Abanes-De Mello, A., Perez, A., Sun, Y.L. Pogliano, K. (1999) A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol Microbiol 31 : 1149 1159.
51. Price, K.D. Losick, R. (1999) A four-dimensional view of assembly of a morphogenetic protein during sporulation in Bacillus subtilis. J Bacteriol 181 : 781 790.
52. Ragkousi, K., Eichenberger, P., van Ooij, C. Setlow, P. (2003) Identification of a new gene essential for germination of Bacillus subtilis spores with Ca2+-dipicolinate. J Bacteriol 185 : 2315 2329.
53. Ramamurthi, K.S. Losick, R. (2008) ATP-driven self-assembly of a morphogenetic protein in Bacillus subtilis. Mol Cell 31 : 406 414.
54. Ramamurthi, K.S., Clapham, K.R. Losick, R. (2006) Peptide anchoring spore coat assembly to the outer forespore membrane in Bacillus subtilis. Mol Microbiol 62 : 1547 1557.
55. Ramamurthi, K.S., Lecuyer, S., Stone, H.A. Losick, R. (2009) Geometric cue for protein localization in a bacterium. Science 323 : 1354 1357.
56. Roels, S., Driks, A. Losick, R. (1992) Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis. J Bacteriol 174 : 575 585.
57. Sacco, M., Ricca, E., Losick, R. Cutting, S. (1995) An additional GerE-controlled gene encoding an abundant spore coat protein from Bacillus subtilis. J Bacteriol 177 : 372 377.
58. Setlow, P. (2003) Spore germination. Curr Opin Microbiol 6 : 550 556.
59. Sharp, M.D. Pogliano, K. (1999) An in vivo membrane fusion assay implicates SpoIIIE in the final stages of engulfment during Bacillus subtilis sporulation. Proc Natl Acad Sci USA 96 : 14553 14558.
60. Skerra, A. (2008) Alternative binding proteins: anticalins - harnessing the structural plasticity of the lipocalin ligand pocket to engineer novel binding activities. FEBS J 275 : 2677 2683.
61. Steichen, C.T., Kearney, J.F. Turnbough, C.L., Jr (2007) Non-uniform assembly of the Bacillus anthracis exosporium and a bottle cap model for spore germination and outgrowth. Mol Microbiol 64 : 359 367.
62. Steil, L., Serrano, M., Henriques, A.O. Volker, U. (2005) Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis. Microbiology 151 : 399 420.
63. Stephenson, K. Hoch, J.A. (2002) Evolution of signalling in the sporulation phosphorelay. Mol Microbiol 46 : 297 304.
64. Sterlini, J.M. Mandelstam, J. (1969) Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance. Biochem J 113 : 29 37.
65. Stragier, P. Losick, R. (1996) Molecular genetics of sporulation in Bacillus subtilis. Annu Rev Genet 30 : 297 241.
66. Takamatsu, H., Kodama, T., Nakayama, T. Watabe, K. (1999) Characterization of the yrbA gene of Bacillus subtilis, involved in resistance and germination of spores. J Bacteriol 181 : 4986 4994.
67. Tars, K., Fridborg, K., Bundule, M. Liljas, L. (2000) The three-dimensional structure of bacteriophage PP7 from Pseudomonas aeruginosa at 3.7-A resolution. Virology 272 : 331 337. (Pubitemid 30480193)
68. Webb, C.D., Decatur, A., Teleman, A. Losick, R. (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.
69. Woods, D.R. Jones, D.T. (1986) Physiological responses of Bacteroides and Clostridium strains to environmental stress factors. Adv Microb Physiol 27 : 1 64.
70. Youngman, P., Perkins, J.B. Losick, R. (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 transposon-borne erm gene. Plasmid 12 : 1 9.
71. Zhang, J., Fitz-James, P.C. Aronson, A.I. (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.
72. Zheng, L.B., Donovan, W.P., Fitz-James, P.C. Losick, R. (1988) Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Genes Dev 2 : 1047 1054.