1887

Abstract

Spore formation in is a superb experimental system with which to study some of the most fundamental problems of cellular development and differentiation. Work begun in the 1980s and ongoing today has led to an impressive understanding of the temporal and spatial regulation of sporulation, and the functions of many of the several hundred genes involved. Early in sporulation the cells divide in an unusual asymmetrical manner, to produce a small prespore cell and a much larger mother cell. Aside from developmental biology, this modified division has turned out to be a powerful system for investigation of cell cycle mechanisms, including the components of the division machine, how the machine is correctly positioned in the cell, and how division is coordinated with replication and segregation of the chromosome. Insights into these fundamental mechanisms have provided opportunities for the discovery and development of novel antibiotics. This review summarizes how the bacterial cell cycle field has developed over the last 20 or so years, focusing on opportunities emerging from the system.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.035634-0
2010-01-01
2020-07-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/1/1.html?itemId=/content/journal/micro/10.1099/mic.0.035634-0&mimeType=html&fmt=ahah

References

  1. Adams D. W., Errington J.. 2009; Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol7:642–653
    [Google Scholar]
  2. Anagnostopoulos C., Spizizen J.. 1961; Requirements for transformation in Bacillus subtilis. J Bacteriol81:741–746
    [Google Scholar]
  3. Bartosik A. A., Mierzejewska J., Thomas C. M., Jagura-Burdzy G.. 2009; ParB deficiency in Pseudomonas aeruginosa destabilizes the partner protein ParA and affects a variety of physiological parameters. Microbiology155:1080–1092
    [Google Scholar]
  4. Bath J., Wu L. J., Errington J., Wang J. C.. 2000; Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science290:995–997
    [Google Scholar]
  5. Ben-Yehuda S., Rudner D. Z., Losick R.. 2003; RacA, a bacterial protein that anchors chromosomes to the cell poles. Science299:532–536
    [Google Scholar]
  6. Ben-Yehuda S., Fujita M., Liu X. S., Gorbatyuk B., Skoko D., Yan J., Marko J. F., Liu J. S., Eichenberger P.. other authors 2005; Defining a centromere-like element in Bacillus subtilis by identifying the binding sites for the chromosome-anchoring protein RacA. Mol Cell17:773–782
    [Google Scholar]
  7. Bigot S., Sivanathan V., Possoz C., Barre F. X., Cornet F.. 2007; FtsK, a literate chromosome segregation machine. Mol Microbiol64:1434–1441
    [Google Scholar]
  8. Bramkamp M., Emmins R., Weston L., Donovan C., Daniel R. A., Errington J.. 2008; A novel component of the division-site selection system of Bacillus subtilis and a new mode of action for the division inhibitor MinCD. Mol Microbiol70:1556–1569
    [Google Scholar]
  9. Breier A. M., 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 Microbiol64:703–718
    [Google Scholar]
  10. Burbulys D., Trach K. A., Hoch J. A.. 1991; Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell64:545–552
    [Google Scholar]
  11. Burkholder W. F., Kurtser I., Grossman A. D.. 2001; Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell104:269–279
    [Google Scholar]
  12. Dajkovic A., Lan G., Sun S. X., Wirtz D., Lutkenhaus J.. 2008; MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr Biol18:235–244
    [Google Scholar]
  13. Daniel R. A., Errington J.. 2003; Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell113:767–776
    [Google Scholar]
  14. Dawes I. W., Kay D., Mandelstam J.. 1971; Determining effect of growth medium on the shape and position of daughter chromosomes and on sporulation in Bacillus subtilis. Nature230:567–569
    [Google Scholar]
  15. Duncker B. P., Chesnokov I. N., McConkey B. J.. 2009; The origin recognition complex protein family. Genome Biol10:214
    [Google Scholar]
  16. Dunn G., Torgersen D. M., Mandelstam J.. 1976; Order of expression of genes affecting septum location during sporulation of Bacillus subtilis. J Bacteriol125:776–779
    [Google Scholar]
  17. Dunn G., Jeffs P., Mann N. H., Torgersen D. M., Young M.. 1978; The relationship between DNA replication and the induction of sporulation in Bacillus subtilis. J Gen Microbiol108:189–195
    [Google Scholar]
  18. Edwards D. H., Errington J.. 1997; The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol24:905–915
    [Google Scholar]
  19. Edwards D. H., Thomaides H. B., Errington J.. 2000; Promiscuous targeting of Bacillus subtilis cell division protein DivIVA to division sites in Escherichia coli and fission yeast. EMBO J19:2719–2727
    [Google Scholar]
  20. Errington J.. 1984; Efficient Bacillus subtilis cloning system using bacteriophage vector ∅105J9. J Gen Microbiol130:2615–2628
    [Google Scholar]
  21. Errington J.. 1993; Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol Rev57:1–33
    [Google Scholar]
  22. Errington J.. 2003; Regulation of endospore formation in Bacillus subtilis. Nat Rev Microbiol1:117–126
    [Google Scholar]
  23. Errington J., Illing N.. 1992; Establishment of cell-specific transcription during sporulation in Bacillus subtilis. Mol Microbiol6:689–695
    [Google Scholar]
  24. Errington J., Jones D.. 1987; Cloning in Bacillus subtilis by transfection with bacteriophage vector φ105J27: isolation and preliminary characterization of transducing phages for 23 sporulation loci. J Gen Microbiol133:493–502
    [Google Scholar]
  25. Fogel M. A., Waldor M. K.. 2006; A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev20:3269–3282
    [Google Scholar]
  26. Fort P., Piggot P. J.. 1984; Nucleotide sequence of sporulation locus spoIIA in Bacillus subtilis. J Gen Microbiol130:2147–2153
    [Google Scholar]
  27. Foulger D., Errington J.. 1989; The role of the sporulation gene spoIIIE in the regulation of prespore-specific gene expression in Bacillus subtilis. Mol Microbiol3:1247–1255
    [Google Scholar]
  28. 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 Dev11:1160–1168
    [Google Scholar]
  29. Gregory J. A., Becker E. C., Pogliano K.. 2008; Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes Dev22:3475–3488
    [Google Scholar]
  30. Gruber S., Errington J.. 2009; Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell137:685–696
    [Google Scholar]
  31. Hauser P. M., Errington J.. 1995; Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis. J Bacteriol177:3923–3931
    [Google Scholar]
  32. Haydon D. J., Stokes N. R., Ure R., Galbraith G., Bennett J. M., Brown D. R., Baker P. J., Barynin V. V., Rice D. W.. other authors 2008; An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science321:1673–1675
    [Google Scholar]
  33. Hempel A. M., Wang S. B., Letek M., Gil J. A., Flärdh K.. 2008; Assemblies of DivIVA mark sites for hyphal branching and can establish new zones of cell wall growth in Streptomyces coelicolor. J Bacteriol190:7579–7583
    [Google Scholar]
  34. Hester C. M., Lutkenhaus J.. 2007; Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci U S A104:20326–20331
    [Google Scholar]
  35. Hilbert D. W., Piggot P. J.. 2004; Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol Mol Biol Rev68:234–262
    [Google Scholar]
  36. Hranueli D., Piggot P. J., Mandelstam J.. 1974; Statistical estimate of the total number of operons specific for Bacillus subtilis sporulation. J Bacteriol119:684–690
    [Google Scholar]
  37. Hu Z., Lutkenhaus J.. 1999; Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol34:82–90
    [Google Scholar]
  38. Hudson D. F., Marshall K. M., Earnshaw W. C.. 2009; Condensin: architect of mitotic chromosomes. Chromosome Res17:131–144
    [Google Scholar]
  39. Ireton K., Gunther N. W. I., Grossman A. D.. 1994; spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol176:5320–5329
    [Google Scholar]
  40. Jenkinson H. F., Mandelstam J.. 1983; Cloning of the Bacillus subtilis lys and spoIIIB genes in phage φ105. J Gen Microbiol129:2229–2240
    [Google Scholar]
  41. Jones D., Errington J.. 1987; Construction of improved bacteriophage φ105 vectors for cloning by transfection in Bacillus subtilis. J Gen Microbiol133:483–492
    [Google Scholar]
  42. Jones L. J. F., Carballido-López R., Errington J.. 2001; Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell104:913–922
    [Google Scholar]
  43. Karmazyn-Campelli C., Bonamy C., Savelli B., Stragier P.. 1989; Tandem genes encoding σ-factors for consecutive steps of development in Bacillus subtilis. Genes Dev3:150–157
    [Google Scholar]
  44. Kim H. J., Calcutt M. J., Schmidt F. J., Chater K. F.. 2000; Partitioning of the linear chromosome during sporulation of Streptomyces coelicolor A3(2) involves an oriC-linked parAB locus. J Bacteriol182:1313–1320
    [Google Scholar]
  45. Kroos L.. 2007; The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet41:13–39
    [Google Scholar]
  46. Leaver M., Domínguez-Cuevas P., Coxhead J. M., Daniel R. A., Errington J.. 2009; Life without a wall or division machine in Bacillus subtilis. Nature457:849–853
    [Google Scholar]
  47. 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 Microbiol60:853–869
    [Google Scholar]
  48. Lenarcic R., Halbedel S., Visser L., Shaw M., Wu L. J., Errington J., Marenduzzo D., Hamoen L. W.. 2009; Localisation of DivIVA by targeting to negatively curved membranes. EMBO J28:2272–2282
    [Google Scholar]
  49. Leonard T. A., Butler P. J., Löwe J.. 2005; Bacterial chromosome segregation: structure and DNA binding of the Soj dimer – a conserved biological switch. EMBO J24:270–282
    [Google Scholar]
  50. Lewis P. J., Partridge S. R., Errington J.. 1994; σ factors, asymmetry, and the determination of cell fate in Bacillus subtilis. Proc Natl Acad Sci U S A91:3849–3853
    [Google Scholar]
  51. Lin D. C.-H., Grossman A. D.. 1998; Identification and characterization of a bacterial chromosome partitioning site. Cell92:675–685
    [Google Scholar]
  52. Lin D. C.-H., Levin P. A., Grossman A. D.. 1997; Bipolar localization of a chromosome partition protein in Bacillus subtilis. Proc Natl Acad Sci U S A94:4721–4726
    [Google Scholar]
  53. Livny J., Yamaichi Y., Waldor M. K.. 2007; Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol189:8693–8703
    [Google Scholar]
  54. Lutkenhaus J.. 2007; Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem76:539–562
    [Google Scholar]
  55. Marston A. L., Errington J.. 1999a; Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol Microbiol33:84–96
    [Google Scholar]
  56. Marston A. L., Errington J.. 1999b; Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell4:673–682
    [Google Scholar]
  57. Marston A. L., Thomaides H. B., Edwards D. H., Sharpe M. E., Errington J.. 1998; Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev12:3419–3430
    [Google Scholar]
  58. Mohl D. A., Easter J., Gober J. W.. 2001; The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus. Mol Microbiol42:741–755
    [Google Scholar]
  59. Møller-Jensen J., Jensen R. B., Gerdes H.. 2000; Plasmid and chromosome segregation in prokaryotes. Trends Microbiol8:313–320
    [Google Scholar]
  60. Murray H., Errington J.. 2008; Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell135:74–84
    [Google Scholar]
  61. Murray H., Ferreira H., Errington J.. 2006; The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol61:1352–1361
    [Google Scholar]
  62. Niki H., Yamaichi Y., Hiraga S.. 2000; Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev14:212–223
    [Google Scholar]
  63. Patrick J. E., Kearns D. B.. 2008; MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol Microbiol70:1166–1179
    [Google Scholar]
  64. Piggot P. J., Coote J. G.. 1976; Genetic aspects of bacterial endospore formation. Bacteriol Rev40:908–962
    [Google Scholar]
  65. Pogliano J., Osborne N., Sharpe 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 Microbiol31:1149–1159
    [Google Scholar]
  66. Quisel J. D., Lin D. C.-H., Grossman A. D.. 1999; Control of development by altered localization of a transcription factor in B. subtilis. Mol Cell4:665–672
    [Google Scholar]
  67. Rahn-Lee L., Gorbatyuk B., Skovgaard O., Losick R.. 2009; The conserved sporulation protein YneE inhibits DNA replication in Bacillus subtilis. J Bacteriol191:3736–3739
    [Google Scholar]
  68. Raskin D. M., De Boer P. A. J.. 1999; MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol181:6419–6424
    [Google Scholar]
  69. Rothfield L., Taghbalout A., Shih Y. L.. 2005; Spatial control of bacterial division-site placement. Nat Rev Microbiol3:959–968
    [Google Scholar]
  70. Sharpe M. E., Errington J.. 1996; The Bacillus subtilis soj-spo0J locus is required for a centromere-like function involved in prespore chromosome partitioning. Mol Microbiol21:501–509
    [Google Scholar]
  71. Shen B., Lutkenhaus J.. 2009; The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinC(C)/MinD. Mol Microbiol72:410–424
    [Google Scholar]
  72. Sterlini J. M., Mandelstam J.. 1969; Commitment to sporulation in Bacillus subtilis and its relationship to the development of actinomycin resistance. Biochem J113:29–37
    [Google Scholar]
  73. Stokes N. R., Sievers J., Barker S., Bennett J. M., Brown D. R., Collins I., Errington V. M., Foulger D., Hall M.. other authors 2005; Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay. J Biol Chem280:39709–39715
    [Google Scholar]
  74. Stragier P., Bouvier J., Bonamy C., Szulmajster J.. 1984; A developmental gene product of Bacillus subtilis homologous to the sigma factor of Escherichia coli. Nature312:376–378
    [Google Scholar]
  75. Sullivan N. L., Marquis K. A., Rudner D. Z.. 2009; Recruitment of SMC by ParB- parS organizes the origin region and promotes efficient chromosome segregation. Cell137:697–707
    [Google Scholar]
  76. Sun D., Fajardo-Cavazos P., Sussman M. D., Tovar-Rojo F., Cabrera-Martinez R.-M., Setlow P.. 1991; Effect of chromosome location of Bacillus subtilis forespore genes on their spo gene dependence and transcription by E σF: identification of features of good E σF-dependent promoters. J Bacteriol173:7867–7874
    [Google Scholar]
  77. Thomaides H. B., Freeman M., El Karoui M., Errington J.. 2001; Division-site-selection protein DivIVA of Bacillus subtilis has a second distinct function in chromosome segregation during sporulation. Genes Dev15:1662–1673
    [Google Scholar]
  78. Veening J. W., Murray H., Errington J.. 2009; A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis. Genes Dev23:1959–1970
    [Google Scholar]
  79. 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 U S A101:9257–9262
    [Google Scholar]
  80. Wagner J. K., Marquis K. A., Rudner D. Z.. 2009; SirA enforces diploidy by inhibiting the replication initiator DnaA during spore formation in Bacillus subtilis. Mol Microbiol73:963–974
    [Google Scholar]
  81. Wang X., Possoz C., Sherratt D. J.. 2005; Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev19:2367–2377
    [Google Scholar]
  82. Wu L. J., Errington J.. 1994; Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science264:572–575
    [Google Scholar]
  83. Wu L. J., Errington J.. 1998; Use of asymmetric cell division and spoIIIE mutants to probe chromosome orientation and organization in Bacillus subtilis. Mol Microbiol27:777–786
    [Google Scholar]
  84. Wu L. J., Errington J.. 2002; A large dispersed chromosomal region required for chromosome segregation in sporulating cells of Bacillus subtilis. EMBO J21:4001–4011
    [Google Scholar]
  85. Wu L. J., Errington J.. 2003; RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol Microbiol49:1463–1475
    [Google Scholar]
  86. Wu L. J., Errington J.. 2004; Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell117:915–925
    [Google Scholar]
  87. Wu L. J., Lewis P. J., Allmansberger R., Hauser P. M., Errington J.. 1995; A conjugation-like mechanism for prespore chromosome partitioning during sporulation in Bacillus subtilis. Genes Dev9:1316–1326
    [Google Scholar]
  88. Wu L. J., Ishikawa S., Kawai Y., Oshima T., Ogasawara N., Errington J.. 2009; Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J28:1940–1952
    [Google Scholar]
  89. Yamaichi Y., Niki H.. 2000; Active segregation by the Bacillus subtilis partitioning system in Escherichia coli. Proc Natl Acad Sci U S A97:14656–14661
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.035634-0
Loading
/content/journal/micro/10.1099/mic.0.035634-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error