Chromosome architecture is a key element of bacterial cellular organization

Cellular Microbiology

Volumn 15, Issue 1, 2013, Pages 45-52

  Ptacin, Jerod L ^a   Shapiro, Lucy ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL CHROMOSOME; BACTERIAL MEMBRANE; BINDING SITE; CELL DIVISION; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CYTOARCHITECTURE; CYTOPLASM; GENE EXPRESSION; GENOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY SEQUENCE; REVIEW;

BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; CHROMOSOMES, BACTERIAL; DNA, BACTERIAL; MODELS, BIOLOGICAL;

BACTERIA (MICROORGANISMS);

EID: 84871044086     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12049     Document Type: Review

References (63)

1. Becker, E.C., and Pogliano, K. (2007) Cell-specific SpoIIIE assembly and DNA translocation polarity are dictated by chromosome orientation. Mol Microbiol 66: 1066-1079.
2. Ben-Yehuda, S., Rudner, D.Z., and Losick, R. (2003a) RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299: 532-536.
3. Ben-Yehuda, S., Rudner, D.Z., and Losick, R. (2003b) Assembly of the SpoIIIE DNA translocase depends on chromosome trapping in Bacillus subtilis. Curr Biol 13: 2196-2200.
4. Ben-Yehuda, S., Fujita, M., Liu, X.S., Gorbatyuk, B., Skoko, D., Yan, J., etal. (2005) Defining a centromere-like element in Bacillus subtilis by identifying the binding sites for the chromosome-anchoring protein RacA. Mol Cell 17: 773-782.
5. Berlatzky, I.A., Rouvinski, A., and Ben-Yehuda, S. (2008) Spatial organization of a replicating bacterial chromosome. Proc Natl Acad Sci USA 105: 14136-14140.
6. Bernhardt, T.G., and de Boer, P.A. (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E.coli. Mol Cell 18: 555-564.
7. Bowman, G.R., Comolli, L.R., Zhu, J., Eckart, M., Koenig, M., Downing, K.H., etal. (2008) A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134: 945-955.
8. Bowman, G.R., Comolli, L.R., Gaietta, G.M., Fero, M., Hong, S.H., Jones, Y., etal. (2010) Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function. Mol Microbiol 76: 173-189.
9. Bramkamp, M., and van Baarle, S. (2009) Division site selection in rod-shaped bacteria. Curr Opin Microbiol 12: 683-688.
10. Breier, A.M., and Grossman, A.D. (2007) Whole-genome analysis of the chromosome partitioning and sporulation protein Spo0J (ParB) reveals spreading and origin-distal sites on the Bacillus subtilis chromosome. Mol Microbiol 64: 703-718.
11. Browning, D.F., Grainger, D.C., and Busby, S.J. (2010) Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 13: 773-780.
12. Butan, C., Hartnell, L.M., Fenton, A.K., Bliss, D., Sockett, R.E., Subramaniam, S., and Milne, J.L. (2011) Spiral architecture of the nucleoid in Bdellovibrio bacteriovorus. J Bacteriol 193: 1341-1350.
13. Cho, H., McManus, H.R., Dove, S.L., and Bernhardt, T.G. (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci USA 108: 3773-3778.
14. Danilova, O., Reyes-Lamothe, R., Pinskaya, M., Sherratt, D., and Possoz, C. (2007) MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 65: 1485-1492.
15. Ebersbach, G., Briegel, A., Jensen, G.J., and Jacobs-Wagner, C. (2008) A self-associating protein critical for chromosome attachment, division, and polar organization in Caulobacter. Cell 134: 956-968.
16. Espeli, O., Borne, R., Dupaigne, P., Thiel, A., Gigant, E., Mercier, R., and Boccard, F.A. (2012) MatP-divisome interaction coordinates chromosome segregation with cell division in E.coli. EMBO J 31: 3198-3211.
17. Fogel, M.A., and Waldor, M.K. (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20: 3269-3282.
18. Fuerst, J.A. (2005) Intracellular compartmentation in Planctomycetes. Annu Rev Microbiol 59: 299-328.
19. Gruber, S., and Errington, J. (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B.subtilis. Cell 137: 685-696.
20. Hui, M.P., Galkin, V.E., Yu, X., Stasiak, A.Z., Stasiak, A., Waldor, M.K., and Egelman, E.H. (2010) ParA2, a Vibrio cholerae chromosome partitioning protein, forms left-handed helical filaments on DNA. Proc Natl Acad Sci USA 107: 4590-4595.
21. Jensen, R.B., Wang, S.C., and Shapiro, L. (2001) A moving DNA replication factory in Caulobacter crescentus. EMBO J 20: 4952-4963.
22. Kiekebusch, D., Michie, K.A., Essen, L.O., Lowe, J., and Thanbichler, M. (2012) Localized dimerization and nucleoid binding drive gradient formation by the bacterial cell division inhibitor MipZ. Mol Cell 46: 245-259.
23. Lenarcic, R., Halbedel, S., Visser, L., Shaw, M., Wu, L.J., Errington, J., etal. (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28: 2272-2282.
24. Leonard, T.A., Butler, P.J., and Lowe, J. (2004) Structural analysis of the chromosome segregation protein Spo0J from Thermus thermophilus. Mol Microbiol 53: 419-432.
25. Leonard, T.A., Butler, P.J., and Lowe, J. (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer-a conserved biological switch. EMBO J 24: 270-282.
26. Lin, D.C., and Grossman, A.D. (1998) Identification and characterization of a bacterial chromosome partitioning site. Cell 92: 675-685.
27. Losick, R., and Stragier, P. (1992) Crisscross regulation of cell-type-specific gene expression during development in B.subtilis. Nature 355: 601-604.
28. McGrath, P.T., Iniesta, A.A., Ryan, K.R., Shapiro, L., and McAdams, H.H. (2006) A dynamically localized protease complex and a polar specificity factor control a cell cycle master regulator. Cell 124: 535-547.
29. Marczynski, G.T., and Shapiro, L. (2002) Control of chromosome replication in Caulobacter crescentus. Annu Rev Microbiol 56: 625-656.
30. Marquis, K.A., Burton, B.M., Nollmann, M., Ptacin, J.L., Bustamante, C., Ben-Yehuda, S., and Rudner, D. (2008) SpoIIIE strips proteins off the DNA during chromosome translocation. Genes Dev 22: 1786-1795.
31. Mercier, R., Petit, M.A., Schbath, S., Robin, S., El Karoui, M., Boccard, F., and Espeli, O. (2008) The MatP/matS site-specific system organizes the terminus region of the E.coli chromosome into a macrodomain. Cell 135: 475-485.
32. Mohl, D.A., and Gober, J.W. (1997) Cell cycle-dependent polar localization of chromosome partitioning proteins in Caulobacter crescentus. Cell 88: 675-684.
33. Montero Llopis, P., Jackson, A.F., Sliusarenko, O., Surovtsev, I., Heinritz, J., Emonet, T., and Jacobs-Wagner, C. (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466: 77-81.
34. Murray, H., Ferreira, H., and Errington, J. (2006) The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 61: 1352-1361.
35. Nevo-Dinur, K., Nussbaum-Shochat, A., Ben-Yehuda, S., and Amster-Choder, O. (2011) Translation-independent localization of mRNA in E.coli. Science 331: 1081-1084.
36. Nielsen, H.J., Ottesen, J.R., Youngren, B., Austin, S.J., and Hansen, F.G. (2006) The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Mol Microbiol 62: 331-338.
37. Ptacin, J.L., Nollmann, M., Becker, E.C., Cozzarelli, N.R., Pogliano, K., and Bustamante, C. (2008) Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis. Nat Struct Mol Biol 15: 485-493.
38. Ptacin, J.L., Lee, S.F., Garner, E.C., Toro, E., Eckart, M., Comolli, L.R., etal. (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12: 791-798.
39. Quon, K.C., Yang, B., Domian, I.J., Shapiro, L., and Marczynski, G.T. (1998) Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci USA 95: 120-125.
40. Ragkousi, K., Cowan, A.E., Ross, M.A., and Setlow, P. (2000) Analysis of nucleoid morphology during germination and outgrowth of spores of Bacillus species. J Bacteriol 182: 5556-5562.
41. Rimsky, S., and Travers, A. (2011) Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins. Curr Opin Microbiol 14: 136-141.
42. Ringgaard, S., van Zon, J., Howard, M., and Gerdes, K. (2009) Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA 106: 19369-19374.
43. Roberts, M.A., Wadhams, G.H., Hadfield, K.A., Tickner, S., and Armitage, J.P. (2012) ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes. Proc Natl Acad Sci USA 109: 6698-6703.
44. Robinow, C., and Kellenberger, E. (1994) The bacterial nucleoid revisited. Microbiol Rev 58: 211-232.
45. Rodionov, O., and Yarmolinsky, M. (2004) Plasmid partitioning and the spreading of P1 partition protein ParB. Mol Microbiol 52: 1215-1223.
46. Ryter, A., Schaeffer, P., and Ionesco, H. (1966) [Cytologic classification, by their blockage stage, of sporulation mutants of Bacillus subtilis Marburg]. Ann Inst Pasteur (Paris) 110: 305-315.
47. Savage, D.F., Afonso, B., Chen, A.H., and Silver, P.A. (2010) Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327: 1258-1261.
48. Schofield, W.B., Lim, H.C., and Jacobs-Wagner, C. (2010) Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J 29: 3068-3081.
49. Sullivan, N.L., Marquis, K.A., and Rudner, D.Z. (2009) Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137: 697-707.
50. Thanbichler, M., and Shapiro, L. (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126: 147-162.
51. Thiel, A., Valens, M., Vallet-Gely, I., Espeli, O., and Boccard, F. (2012) Long-range chromosome organization in E.coli: a site-specific system isolates the Ter macrodomain. PLoS Genet 8: e1002672.
52. Tonthat, N.K., Arold, S.T., Pickering, B.F., Van Dyke, M.W., Liang, S., Lu, Y., etal. (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30: 154-164.
53. Toro, E., Hong, S.H., McAdams, H.H., and Shapiro, L. (2008) Caulobacter requires a dedicated mechanism to initiate chromosome segregation. Proc Natl Acad Sci USA 105: 15435-15440.
54. Umbarger, M.A., Toro, E., Wright, M.A., Porreca, G.J., Bau, D., Hong, S.H., etal. (2011) The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol Cell 44: 252-264.
55. Vecchiarelli, A.G., Han, Y.W., Tan, X., Mizuuchi, M., Ghirlando, R., Biertumpfel, C., etal. (2010) ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition. Mol Microbiol 78: 78-91.
56. Veiga, H., Jorge, A.M., and Pinho, M.G. (2011) Absence of nucleoid occlusion effector Noc impairs formation of orthogonal FtsZ rings during Staphylococcus aureus cell division. Mol Microbiol 80: 1366-1380.
57. Viollier, P.H., Thanbichler, M., McGrath, P.T., West, L., Meewan, M., McAdams, H.H., and 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.
58. Wagner-Herman, J.K., Bernard, R., Dunne, R., Bisson-Filho, A.W., Kumar, K., Nguyen, T., etal. (2012) RefZ facilitates the switch from medial to polar division during spore formation in Bacillus subtilis. J Bacteriol 194: 4608-4618.
59. Wang, X., Liu, X., Possoz, C., and Sherratt, D.J. (2006) The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev 20: 1727-1731.
60. Werner, J.N., Chen, E.Y., Guberman, J.M., Zippilli, A.R., Irgon, J.J., and Gitai, Z. (2009) Quantitative genome-scale analysis of protein localization in an asymmetric bacterium. Proc Natl Acad Sci USA 106: 7858-7863.
61. Wu, L.J., and Errington, J. (2003) RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol Microbiol 49: 1463-1475.
62. Wu, L.J., and Errington, J. (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915-925.
63. Wu, L.J., Ishikawa, S., Kawai, Y., Oshima, T., Ogasawara, N., and Errington, J. (2009) Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J 28: 1940-1952.