Whole-genome analysis of the chromosome partitioning and sporulation protein Spo0J (ParB) reveals spreading and origin-distal sites on the Bacillus subtilis chromosome

Molecular Microbiology

Volumn 64, Issue 3, 2007, Pages 703-718

  Breier, Adam M ^a   Grossman, Alan D ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN PAR A; PROTEIN PAR B; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL GROWTH; CHROMOSOME ANALYSIS; CONSENSUS SEQUENCE; CONTROLLED STUDY; DNA BINDING; GENE DELETION; GENE EXPRESSION PROFILING; GENE INTERACTION; GENE LOCUS; GENETIC SIMILARITY; GENETIC TRANSCRIPTION; GENOME ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; MUTANT; NONHUMAN; NULL ALLELE; PHENOTYPE; PRIORITY JOURNAL; SPOROGENESIS; WILD TYPE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMES, BACTERIAL; DNA REPLICATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENOME, BACTERIAL; MICROSCOPY, FLUORESCENCE; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN BINDING; TRANSCRIPTION, GENETIC;

BACILLUS SUBTILIS;

EID: 34247497733     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05690.x     Document Type: Article

References (64)

1. Au, N., Kuester-Schoeck, E., Mandava, V., Bothwell, L.E., Canny, S.P., Chachu, K., et al. (2005) Genetic composition of the Bacillus subtilis SOS system. J Bacteriol 187 : 7655 7666.
2. Auchtung, J.M., Lee, C.A., Monson, R.E., Lehman, A.P. Grossman, A.D. (2005) Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci USA 102 : 12554 12559.
3. Bartosik, A.A., Lasocki, K., Mierzejewska, J., Thomas, C.M. Jagura-Burdzy, G. (2004) ParB of Pseudomonas aeruginosa: interactions with its partner ParA and its target parS and specific effects on bacterial growth. J Bacteriol 186 : 6983 6998.
4. Bingle, L.E., Macartney, D.P., Fantozzi, A., Manzoor, S.E. Thomas, C.M. (2005) Flexibility in repression and cooperativity by KorB of broad host range IncP-1 plasmid RK2. J Mol Biol 349 : 302 316.
5. Britton, R.A. Grossman, A.D. (1999) Synthetic lethal phenotypes caused by mutations affecting chromosome partitioning in Bacillus subtilis. J Bacteriol 181 : 5860 5864.
6. Britton, R.A., Lin, D.C. Grossman, A.D. (1998) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12 : 1254 1259.
7. Britton, R.A., Eichenberger, P., Gonzalez-Pastor, J.E., Fawcett, P., Monson, R., Losick, R. Grossman, A.D. (2002) Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J Bacteriol 184 : 4881 4890.
8. Bulyk, M.L. (2006) DNA microarray technologies for measuring protein-DNA interactions. Curr Opin Biotechnol 17 : 422 430.
9. Cervin, M.A., Spiegelman, G.B., Raether, B., Ohlsen, K., Perego, M. Hoch, J.A. (1998) A negative regulator linking chromosome segregation to developmental transcription in Bacillus subtilis. Mol Microbiol 29 : 85 95.
10. Crooks, G.E., Hon, G., Chandonia, J.M. Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res 14 : 1188 1190.
11. Dubarry, N., Pasta, F. Lane, D. (2006) ParABS systems of the four replicons of Burkholderia cenocepacia: new chromosome centromeres confer partition specificity. J Bacteriol 188 : 1489 1496.
12. Easter, J. Gober, J.W. (2002) ParB-stimulated nucleotide exchange regulates a switch in functionally distinct ParA activities. Mol Cell 10 : 427 434.
13. Fogel, M.A. Waldor, M.K. (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20 : 3269 3282.
14. Friedman, S.A. Austin, S.J. (1988) The P1 plasmid-partition system synthesizes two essential proteins from an autoregulated operon. Plasmid 19 : 103 112.
15. Glaser, P., Sharpe, M.E., Raether, B., Perego, M., Ohlsen, K. Errington, J. (1997) Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev 11 : 1160 1168.
16. Goranov, A.I., Katz, L., Breier, A.M., Burge, C.B. Grossman, A.D. (2005) A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA. Proc Natl Acad Sci USA 102 : 12932 12937.
17. Goranov, A.I., Kuester-Schoeck, E., Wang, J.D. Grossman, A.D. (2006) Characterization of the global transcriptional responses to different types of DNA damage and disruption of replication in Bacillus subtilis. J Bacteriol 188 : 5595 5605.
18. Harwood, C.R. Cutting, S.M. (1990) Molecular Biological Methods for Bacillus. Chichester : John Wiley & Sons.
19. Hayes, F. Barilla, D. (2006) Assembling the bacterial segrosome. Trends Biochem Sci 31 : 247 250.
20. Hoch, J.A. Mathews, J.L. (1973) Chromosomal location of pleiotropic negative sporulation mutations in Bacillus subtilis. Genetics 73 : 215 228.
21. Hranueli, D., Piggot, P.J. Mandelstam, J. (1974) Statistical estimate of the total number of operons specific for Bacillus subtilis sporulation. J Bacteriol 119 : 684 690.
22. Huang, X., Decatur, A., Sorokin, A. Helmann, J.D. (1997) The Bacillus subtilis sigma (X) protein is an extracytoplasmic function sigma factor contributing to survival at high temperature. J Bacteriol 179 : 2915 2921.
23. Ireton, K., Gunther, N.W.T. Grossman, A.D. (1994) spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176 : 5320 5329.
24. Jagura-Burdzy, G., Macartney, D.P., Zatyka, M., Cunliffe, L., Cooke, D., Huggins, C., et al. (1999) Repression at a distance by the global regulator KorB of promiscuous IncP plasmids. Mol Microbiol 32 : 519 532.
25. Jakimowicz, D., Chater, K. Zakrzewska-Czerwinska, J. (2002) The ParB protein of Streptomyces coelicolor A3 (2) recognizes a cluster of parS sequences within the origin-proximal region of the linear chromosome. Mol Microbiol 45 : 1365 1377.
26. Jensen, R.B. Shapiro, L. (1999) Chromosome segregation during the prokaryotic cell division cycle. Curr Opin Cell Biol 11 : 726 731.
27. Kalnin, K., Stegalkina, S. Yarmolinsky, M. (2000) pTAR-encoded proteins in plasmid partitioning. J Bacteriol 182 : 1889 1894.
28. Kim, S.K. Wang, J.C. (1999) Gene silencing via protein-mediated subcellular localization of DNA. Proc Natl Acad Sci USA 96 : 8557 8561.
29. Lau, I.F., Filipe, S.R., Soballe, B., Okstad, O.A., Barre, F.X. Sherratt, D.J. (2003) Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol Microbiol 49 : 731 743.
30. Lee, P.S. Grossman, A.D. (2006) The chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillus subtilis. Mol Microbiol 60 : 853 869.
31. Lee, P.S., Lin, D.C., Moriya, S. Grossman, A.D. (2003) Effects of the chromosome partitioning protein Spo0J (ParB) on oriC positioning and replication initiation in Bacillus subtilis. J Bacteriol 185 : 1326 1337.
32. Lemon, K.P. Grossman, A.D. (2001) The extrusion-capture model for chromosome partitioning in bacteria. Genes Dev 15 : 2031 2041.
33. Leonard, T.A., Butler, P.J. Lowe, J. (2004) Structural analysis of the chromosome segregation protein Spo0J from Thermus thermophilus. Mol Microbiol 53 : 419 432.
34. Leonard, T.A., Moller-Jensen, J. Lowe, J. (2005a) Towards understanding the molecular basis of bacterial DNA segregation. Philos Trans R Soc Lond B Biol Sci 360 : 523 535.
35. Leonard, T.A., Butler, P.J. Lowe, J. (2005b) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer - a conserved biological switch. EMBO J 24 : 270 282.
36. Li, Y., Sergueev, K. Austin, S. (2002) The segregation of the Escherichia coli origin and terminus of replication. Mol Microbiol 46 : 985 996.
37. Lin, D.C. (1999) Chromosome paritioning in bacillus subtilis. PhD Thesis, Massachusetts Institute of Technology, Cambridge, MA, USA.
38. Lin, D.C. Grossman, A.D. (1998) Identification and characterization of a bacterial chromosome partitioning site. Cell 92 : 675 685.
39. Lin, D.C., Levin, P.A. Grossman, A.D. (1997) Bipolar localization of a chromosome partition protein in Bacillus subtilis. Proc Natl Acad Sci USA 94 : 4721 4726.
40. Lindow, J.C., Britton, R.A. Grossman, A.D. (2002) Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo. J Bacteriol 184 : 5317 5322.
41. Lukaszewicz, M., Kostelidou, K., Bartosik, A.A., Cooke, G.D., Thomas, C.M. Jagura-Burdzy, G. (2002) Functional dissection of the ParB homologue (KorB) from IncP-1 plasmid RK2. Nucleic Acids Res 30 : 1046 1055.
42. Lynch, A.S. Wang, J.C. (1994) Use of an inducible site-specific recombinase to probe the structure of protein-DNA complexes involved in F plasmid partition in Escherichia coli. J Mol Biol 236 : 679 684.
43. Lynch, A.S. Wang, J.C. (1995) SopB protein-mediated silencing of genes linked to the sopC locus of Escherichia coli F plasmid. Proc Natl Acad Sci USA 92 : 1896 1900.
44. Marston, A.L. Errington, J. (1999) Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell 4 : 673 682.
45. Murray, H., Ferreira, H. Errington, J. (2006) The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 61 : 1352 1361.
46. Ogura, Y., Ogasawara, N., Harry, E.J. Moriya, S. (2003) Increasing the ratio of Soj to Spo0J promotes replication initiation in Bacillus subtilis. J Bacteriol 185 : 6316 6324.
47. Piggot, P.J. Coote, J.G. (1976) Genetic aspects of bacterial endospore formation. Bacteriol Rev 40 : 908 962.
48. Quisel, J.D. Grossman, A.D. (2000) Control of sporulation gene expression in Bacillus subtilis by the chromosome partitioning proteins Soj (ParA) and Spo0J (ParB). J Bacteriol 182 : 3446 3451.
49. Quisel, J.D., Lin, D.C. Grossman, A.D. (1999) Control of development by altered localization of a transcription factor in B. subtilis. Mol Cell 4 : 665 672.
50. Raskin, D.M. de Boer, P.A. (1999) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA 96 : 4971 4976.
51. Rodionov, O., Lobocka, M. Yarmolinsky, M. (1999) Silencing of genes flanking the P1 plasmid centromere. Science 283 : 546 549.
52. Sharpe, M.E. Errington, J. (1998) A fixed distance for separation of newly replicated copies of oriC in Bacillus subtilis: implications for co-ordination of chromosome segregation and cell division. Mol Microbiol 28 : 981 990.
53. Shinagawa, H. (1996) SOS response as an adaptive response to DNA damage in prokaryotes. EXS 77 : 221 235.
54. Surtees, J.A. Funnell, B.E. (1999) P1 ParB domain structure includes two independent multimerization domains. J Bacteriol 181 : 5898 5908.
55. Surtees, J.A. Funnell, B.E. (2003) Plasmid and chromosome traffic control: how ParA and ParB drive partition. Curr Top Dev Biol 56 : 145 180.
56. Teleman, A.A., Graumann, P.L., Lin, D.C., Grossman, A.D. Losick, R. (1998) Chromosome arrangement within a bacterium. Curr Biol 8 : 1102 1109.
57. Tusher, V.G., Tibshirani, R. Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98 : 5116 5121.
58. Viollier, P.H., Thanbichler, M., McGrath, P.T., West, L., Meewan, M., McAdams, H.H. Shapiro, L. (2004) Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Natl Acad Sci USA 101 : 9257 9262.
59. Webb, C.D., Teleman, A., Gordon, S., Straight, A., Belmont, A., Lin, D.C., et al. (1997) Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis. Cell 88 : 667 674.
60. Webb, C.D., Graumann, P.L., Kahana, J.A., Teleman, A.A., Silver, P.A. Losick, R. (1998) Use of time-lapse microscopy to visualize rapid movement of the replication origin region of the chromosome during the cell cycle in Bacillus subtilis. Mol Microbiol 28 : 883 892.
61. Williams, D.R., Motallebi-Veshareh, M. Thomas, C.M. (1993) Multifunctional repressor KorB can block transcription by preventing isomerization of RNA polymerase-promoter complexes. Nucleic Acids Res 21 : 1141 1148.
62. Wu, J., Smith, L.T., Plass, C. Huang, T.H. (2006) ChIP-chip comes of age for genome-wide functional analysis. Cancer Res 66 : 6899 6902.
63. Yamaichi, Y. Niki, H. (2000) Active segregation by the Bacillus subtilis partitioning system in Escherichia coli. Proc Natl Acad Sci USA 97 : 14656 14661.
64. Yates, P., Lane, D. Biek, D.P. (1999) The F plasmid centromere, sopC, is required for full repression of the sopAB operon. J Mol Biol 290 : 627 638.