1887

Abstract

Plasmids are the tools of choice for studying bacterial functions involved in DNA maintenance. Here a genetic study on the replication of a novel, low-copy-number, plasmid, pBS72, is reported. The results show that two plasmid elements, the initiator protein RepA and an iteron-containing origin, and at least nine host-encoded replication proteins, the primosomal proteins DnaB, DnaC, DnaD, DnaG and DnaI, the DNA polymerases DnaE and PolC, and the polymerase cofactors DnaN and DnaX, are required for pBS72 replication. On the contrary, the cellular initiators DnaA and PriA, the helicase PcrA and DNA polymerase I are dispensable. From this, it is inferred that pBS72 replication is of the theta type and is initiated by an original mechanism. Indirect evidence suggests that during this process the DnaC helicase might be delivered to the plasmid origin by the weakly active DnaD pathway stimulated by a predicted interaction between DnaC and a domain of RepA homologous to the major DnaC-binding domain of the cellular initiator DnaA. The plasmid pBS72 replication fork appears to require the same functions as the bacterial chromosome and the unrelated plasmid pAM1. Most importantly, this replication machinery contains the two type C polymerases, PolC and DnaE. As the mechanism of initiation of the three genomes is substantially different, this suggests that both type C polymerases might be required in any Cairns replication in and presumably in other bacteria encoding PolC and DnaE.

Keyword(s): CN, copy number
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2006-05-01
2019-10-14
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References

  1. Abhyankar, M. M., Reddy, J. M., Sharma, R., Bullesbach, E. & Bastia, D. ( 2004; ). Biochemical investigations of control of replication initiation of plasmid R6K. J Biol Chem 279, 6711–6719.
    [Google Scholar]
  2. Anand, S. P., Chattopadhyay, A. & Khan, S. A. ( 2005; ). The PcrA3 mutant binds DNA and interacts with the RepC initiator protein of plasmid pT181 but is defective in its DNA helicase and unwinding activities. Plasmid 54, 104–113.[CrossRef]
    [Google Scholar]
  3. Attolini, C., Mazza, G., Fortunato, A., Ciarrocchi, G., Mastromei, G., Riva, S. & Falaschi, A. ( 1976; ). On the identity of dnaP and dnaF genes of Bacillus subtilis. Mol Gen Genet 148, 9–17.[CrossRef]
    [Google Scholar]
  4. Benkovic, S. J., Valentine, A. M. & Salinas, F. ( 2001; ). Replisome-mediated DNA replication. Annu Rev Biochem 70, 181–208.[CrossRef]
    [Google Scholar]
  5. Bernander, R., Dasgupta, S. & Nordstrom, K. ( 1991; ). The E. coli cell cycle and the plasmid R1 replication cycle in the absence of the DnaA protein. Cell 64, 1145–1153.[CrossRef]
    [Google Scholar]
  6. Bron, S. ( 1990; ). Plasmids. In Molecular Biological Methods for Bacillus, pp. 75–174. Edited by C. R. Harwood & S. M. Cutting. Chichester: Wiley.
  7. Bruand, C., Ehrlich, S. D. & Janniere, L. ( 1995; ). Primosome assembly site in Bacillus subtilis. EMBO J 14, 2642–2650.
    [Google Scholar]
  8. Bruand, C., Farache, M., McGovern, S., Ehrlich, S. D. & Polard, P. ( 2001; ). DnaB, DnaD and DnaI proteins are components of the Bacillus subtilis replication restart primosome. Mol Microbiol 42, 245–255.
    [Google Scholar]
  9. Bruand, C., Velten, M., McGovern, S., Marsin, S., Serena, C., Ehrlich, S. D. & Polard, P. ( 2005; ). Functional interplay between the Bacillus subtilis DnaD and DnaB proteins essential for initiation and re-initiation of DNA replication. Mol Microbiol 55, 1138–1150.
    [Google Scholar]
  10. Bruck, I. & O'Donnell, M. ( 2000; ). The DNA replication machine of a gram-positive organism. J Biol Chem 275, 28971–28983.[CrossRef]
    [Google Scholar]
  11. Bruck, I., Yuzhakov, A., Yurieva, O., Jeruzalmi, D., Skangalis, M., Kuriyan, J. & O'Donnell, M. ( 2002; ). Analysis of a multicomponent thermostable DNA polymerase III replicase from an extreme thermophile. J Biol Chem 277, 17334–17348.[CrossRef]
    [Google Scholar]
  12. Bullock, P. A. ( 1997; ). The initiation of simian virus 40 DNA replication in vitro. Crit Rev Biochem Mol Biol 32, 503–568.[CrossRef]
    [Google Scholar]
  13. Burgers, P. M. ( 1998; ). Eukaryotic DNA polymerases in DNA replication and DNA repair. Chromosoma 107, 218–227.[CrossRef]
    [Google Scholar]
  14. Ceglowski, P., Lurz, R. & Alonso, J. C. ( 1993; ). Functional analysis of pSM19035-derived replicons in Bacillus subtilis. FEMS Microbiol Lett 109, 145–150.[CrossRef]
    [Google Scholar]
  15. Cox, M. M., Goodman, M. F., Kreuzer, K. N., Sherratt, D. J., Sandler, S. J. & Marians, K. J. ( 2000; ). The importance of repairing stalled replication forks. Nature 404, 37–41.[CrossRef]
    [Google Scholar]
  16. Datta, H. J., Khatri, G. S. & Bastia, D. ( 1999; ). Mechanism of recruitment of DnaB helicase to the replication origin of the plasmid pSC101. Proc Natl Acad Sci U S A 96, 73–78.[CrossRef]
    [Google Scholar]
  17. Davey, M. J. & O'Donnell, M. ( 2003; ). Replicative helicase loaders: ring breakers and ring makers. Curr Biol 13, R594–R596.[CrossRef]
    [Google Scholar]
  18. del Solar, G., Giraldo, R., Ruiz-Echevarria, M. J., Espinosa, M. & Diaz-Orejas, R. ( 1998; ). Replication and control of circular bacterial plasmids. Microbiol Mol Biol Rev 62, 434–464.
    [Google Scholar]
  19. Dervyn, E., Suski, C., Daniel, R., Bruand, C., Chapuis, J., Errington, J., Janniere, L. & Ehrlich, S. D. ( 2001; ). Two essential DNA polymerases at the bacterial replication fork. Science 294, 1716–1719.[CrossRef]
    [Google Scholar]
  20. Edgell, D. R. & Doolittle, W. F. ( 1997; ). Archaea and the origin(s) of DNA replication proteins. Cell 89, 995–998.[CrossRef]
    [Google Scholar]
  21. Espinosa, M., Cohen, S., Couturier, M. & 7 other authors ( 2000; ). Plasmid replication and copy number control. In The Horizontal Gene Pool: Bacterial Plasmids and Gene Spread, pp. 1–47. Edited by C. M. Thomas. London: Taylor & Francis.
  22. Felczak, M. M., Simmons, L. A. & Kaguni, J. M. ( 2005; ). An essential tryptophan of Escherichia coli DnaA protein functions in oligomerization at the E. coli replication origin. J Biol Chem 280, 24627–24633.[CrossRef]
    [Google Scholar]
  23. Fukui, T., Yamauchi, K., Muroya, T., Akiyama, M., Maki, H., Sugino, A. & Waga, S. ( 2004; ). Distinct roles of DNA polymerases delta and epsilon at the replication fork in Xenopus egg extracts. Genes Cells 9, 179–191.[CrossRef]
    [Google Scholar]
  24. Garg, P., Stith, C. M., Sabouri, N., Johansson, E. & Burgers, P. M. ( 2004; ). Idling by DNA polymerase delta maintains a ligatable nick during lagging-strand DNA replication. Genes Dev 18, 2764–2773.[CrossRef]
    [Google Scholar]
  25. Giraldo, R. ( 2003; ). Common domains in the initiators of DNA replication in Bacteria, Archaea and Eukarya: combined structural, functional and phylogenetic perspectives. FEMS Microbiol Rev 26, 533–554.[CrossRef]
    [Google Scholar]
  26. Hassan, A. K., Moriya, S., Ogura, M., Tanaka, T., Kawamura, F. & Ogasawara, N. ( 1997; ). Suppression of initiation defects of chromosome replication in Bacillus subtilis dnaA and oriC-deleted mutants by integration of a plasmid replicon into the chromosomes. J Bacteriol 179, 2494–2502.
    [Google Scholar]
  27. Helinski, D. R., Toukdarian, A. E. & Novick, R. P. ( 1996; ). Replication control and other stable maintenance mechanisms of plasmids. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 2295–2324. Edited by F. C. Neidhart. Washington, DC: American Society for Microbiology.
  28. Henneke, G., Flament, D., Hubscher, U., Querellou, J. & Raffin, J. P. ( 2005; ). The hyperthermophilic euryarchaeota Pyrococcus abyssi likely requires the two DNA polymerases D and B for DNA replication. J Mol Biol 350, 53–64.[CrossRef]
    [Google Scholar]
  29. Hubscher, U., Nasheuer, H. P. & Syvaoja, J. E. ( 2000; ). Eukaryotic DNA polymerases, a growing family. Trends Biochem Sci 25, 143–147.[CrossRef]
    [Google Scholar]
  30. Inoue, R., Kaito, C., Tanabe, M., Kamura, K., Akimitsu, N. & Sekimizu, K. ( 2001; ). Genetic identification of two distinct DNA polymerases, DnaE and PolC, that are essential for chromosomal DNA replication in Staphylococcus aureus. Mol Genet Genomics 266, 564–571.[CrossRef]
    [Google Scholar]
  31. Ishigo-Oka, D., Ogasawara, N. & Moriya, S. ( 2001; ). DnaD protein of Bacillus subtilis interacts with DnaA, the initiator protein of replication. J Bacteriol 183, 2148–2150.[CrossRef]
    [Google Scholar]
  32. Johnson, A. & O'Donnell, M. ( 2005; ). Cellular DNA replicases: components and dynamics at the replication fork. Annu Rev Biochem 74, 283–315.[CrossRef]
    [Google Scholar]
  33. Karthikeyan, R., Vonarx, E. J., Straffon, A. F., Simon, M., Faye, G. & Kunz, B. A. ( 2000; ). Evidence from mutational specificity studies that yeast DNA polymerases delta and epsilon replicate different DNA strands at an intracellular replication fork. J Mol Biol 299, 405–419.[CrossRef]
    [Google Scholar]
  34. Kawasaki, Y. & Sugino, A. ( 2001; ). Yeast replicative DNA polymerases and their role at the replication fork. Mol Cells 12, 277–285.
    [Google Scholar]
  35. Kelley, W. L. & Bastia, D. ( 1992; ). Activation in vivo of the minimal replication origin beta of plasmid R6K requires a small target sequence essential for DNA looping. New Biol 4, 569–580.
    [Google Scholar]
  36. Khan, S. A. ( 2005; ). Plasmid rolling-circle replication: highlights of two decades of research. Plasmid 53, 126–136.[CrossRef]
    [Google Scholar]
  37. Konieczny, I. ( 2003; ). Strategies for helicase recruitment and loading in bacteria. EMBO Rep 4, 37–41.[CrossRef]
    [Google Scholar]
  38. Laipis, P. J. & Ganesan, A. T. ( 1972; ). A deoxyribonucleic acid polymerase I-deficient mutant of Bacillus subtilis. J Biol Chem 247, 5867–5871.
    [Google Scholar]
  39. Leipe, D. D., Aravind, L. & Koonin, E. V. ( 1999; ). Did DNA replication evolve twice independently? Nucleic Acids Res 27, 3389–3401.[CrossRef]
    [Google Scholar]
  40. Lemon, K. P. & Grossman, A. D. ( 1998; ). Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282, 1516–1519.[CrossRef]
    [Google Scholar]
  41. Lemon, K. P. & Grossman, A. D. ( 2000; ). Movement of replicating DNA through a stationary replisome. Mol Cell 6, 1321–1330.[CrossRef]
    [Google Scholar]
  42. Lemon, K. P., Moriya, S., Ogasawara, N. & Grossman, A. D. ( 2002; ). Chromosome replication and segregation. In Bacillus subtilis and its Closest Relatives, pp. 73–86. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
  43. Lu, Y. B., Datta, H. J. & Bastia, D. ( 1998; ). Mechanistic studies of initiator–initiator interaction and replication initiation. EMBO J 17, 5192–5200.[CrossRef]
    [Google Scholar]
  44. Marsin, S., McGovern, S., Ehrlich, S. D., Bruand, C. & Polard, P. ( 2001; ). Early steps of Bacillus subtilis primosome assembly. J Biol Chem 276, 45818–45825.[CrossRef]
    [Google Scholar]
  45. Martinez-Jimenez, M. I., Mesa, P. & Alonso, J. C. ( 2002; ). Bacillus subtilis tau subunit of DNA polymerase III interacts with bacteriophage SPP1 replicative DNA helicase G40P. Nucleic Acids Res 30, 5056–5064.[CrossRef]
    [Google Scholar]
  46. Mauel, C. & Karamata, D. ( 1984; ). Prophage induction in thermosensitive DNA mutants of Bacillus subtilis. Mol Gen Genet 194, 451–456.[CrossRef]
    [Google Scholar]
  47. McHenry, C. S. ( 2003; ). Chromosomal replicases as asymmetric dimers: studies of subunit arrangement and functional consequences. Mol Microbiol 49, 1157–1165.[CrossRef]
    [Google Scholar]
  48. Moriya, S., Imai, Y., Hassan, A. K. & Ogasawara, N. ( 1999; ). Regulation of initiation of Bacillus subtilis chromosome replication. Plasmid 41, 17–29.[CrossRef]
    [Google Scholar]
  49. Morrison, A. & Sugino, A. ( 1994; ). The 3′→5′ exonucleases of both DNA polymerases delta and epsilon participate in correcting errors of DNA replication in Saccharomyces cerevisiae. Mol Gen Genet 242, 289–296.[CrossRef]
    [Google Scholar]
  50. Pacek, M., Konopa, G. & Konieczny, I. ( 2001; ). DnaA box sequences as the site for helicase delivery during plasmid RK2 replication initiation in Escherichia coli. J Biol Chem 276, 23639–23644.[CrossRef]
    [Google Scholar]
  51. Park, K., Han, E., Paulsson, J. & Chattoraj, D. K. ( 2001; ). Origin pairing (‘handcuffing’) as a mode of negative control of P1 plasmid copy number. EMBO J 20, 7323–7332.[CrossRef]
    [Google Scholar]
  52. Petit, M. A., Dervyn, E., Rose, M., Entian, K. D., McGovern, S., Ehrlich, S. D. & Bruand, C. ( 1998; ). PcrA is an essential DNA helicase of Bacillus subtilis fulfilling functions both in repair and rolling-circle replication. Mol Microbiol 29, 261–273.[CrossRef]
    [Google Scholar]
  53. Polard, P., Marsin, S., McGovern, S., Velten, M., Wigley, D. B., Ehrlich, S. D. & Bruand, C. ( 2002; ). Restart of DNA replication in Gram-positive bacteria: functional characterisation of the Bacillus subtilis PriA initiator. Nucleic Acids Res 30, 1593–1605.[CrossRef]
    [Google Scholar]
  54. Ratnakar, P. V., Mohanty, B. K., Lobert, M. & Bastia, D. ( 1996; ). The replication initiator protein pi of the plasmid R6K specifically interacts with the host-encoded helicase DnaB. Proc Natl Acad Sci U S A 93, 5522–5526.[CrossRef]
    [Google Scholar]
  55. Rocha, E. ( 2002; ). Is there a role for replication fork asymmetry in the distribution of genes in bacterial genomes? Trends Microbiol 10, 393.[CrossRef]
    [Google Scholar]
  56. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  57. Scherzinger, E., Haring, V., Lurz, R. & Otto, S. ( 1991; ). Plasmid RSF1010 DNA replication in vitro promoted by purified RSF1010 RepA, RepB and RepC proteins. Nucleic Acids Res 19, 1203–1211.[CrossRef]
    [Google Scholar]
  58. Seitz, H., Weigel, C. & Messer, W. ( 2000; ). The interaction domains of the DnaA and DnaB replication proteins of Escherichia coli. Mol Microbiol 37, 1270–1279.[CrossRef]
    [Google Scholar]
  59. Sharma, R., Kachroo, A. & Bastia, D. ( 2001; ). Mechanistic aspects of DnaA-RepA interaction as revealed by yeast forward and reverse two-hybrid analysis. EMBO J 20, 4577–4587.[CrossRef]
    [Google Scholar]
  60. Shcherbakova, P. V. & Pavlov, Y. I. ( 1996; ). 3′→5′ exonucleases of DNA polymerases epsilon and delta correct base analog induced DNA replication errors on opposite DNA strands in Saccharomyces cerevisiae. Genetics 142, 717–726.
    [Google Scholar]
  61. Sugino, A. ( 1995; ). Yeast DNA polymerases and their role at the replication fork. Trends Biochem Sci 20, 319–323.[CrossRef]
    [Google Scholar]
  62. Sutton, M. D., Carr, K. M., Vicente, M. & Kaguni, J. M. ( 1998; ). Escherichia coli DnaA protein. The N-terminal domain and loading of DnaB helicase at the E. coli chromosomal origin. J Biol Chem 273, 34255–34262.[CrossRef]
    [Google Scholar]
  63. Swinfield, T. J., Janniere, L., Ehrlich, S. D. & Minton, N. P. ( 1991; ). Characterization of a region of the Enterococcus faecalis plasmid pAM beta 1 which enhances the segregational stability of pAM beta 1-derived cloning vectors in Bacillus subtilis. Plasmid 26, 209–221.[CrossRef]
    [Google Scholar]
  64. Tang, X. B., Womble, D. D. & Rownd, R. H. ( 1989; ). DnaA protein is not essential for replication of IncFII plasmid NR1. J Bacteriol 171, 5290–5295.
    [Google Scholar]
  65. Titok, M. A., Chapuis, J., Selezneva, Y. V., Lagodich, A. V., Prokulevich, V. A., Ehrlich, S. D. & Janniere, L. ( 2003; ). Bacillus subtilis soil isolates: plasmid replicon analysis and construction of a new theta-replicating vector. Plasmid 49, 53–62.[CrossRef]
    [Google Scholar]
  66. Velten, M., McGovern, S., Marsin, S., Ehrlich, S. D., Noirot, P. & Polard, P. ( 2003; ). A two-protein strategy for the functional loading of a cellular replicative DNA helicase. Mol Cell 11, 1009–1020.[CrossRef]
    [Google Scholar]
  67. Winston, S. A. S. N. ( 1982; ). DNA replication in Bacillus subtilis. In The Molecular Biology of the Bacilli, pp. 35–69. Edited by D. Dubnau. San Diego: Academic Press Inc.
  68. Wright, G. E., Brown, N. C., Xu, W. C., Long, Z. Y., Zhi, C., Gambino, J. J., Barnes, M. H. & Butler, M. M. ( 2005; ). Active site directed inhibitors of replication-specific bacterial DNA polymerases. Bioorg Med Chem Lett 15, 729–732.[CrossRef]
    [Google Scholar]
  69. Yoshikawa, H. & Wake, R. G. ( 1993; ). Initiation and termination of chromosome replication. In Bacillus subtilis and Other Gram-positive Bacteria: Biochemistry, Physiology and Molecular Genetics, pp. 507–528. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington DC: American Society for Microbiology.
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