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. 1986 Jun;83(12):4423–4427. doi: 10.1073/pnas.83.12.4423

Host participation in plasmid maintenance: dependence upon dnaA of replicons derived from P1 and F.

E B Hansen, M B Yarmolinsky
PMCID: PMC323745  PMID: 3520571

Abstract

Nonparticipation of the bacterial dnaA gene in plasmid replication has been assumed to be the general rule. In conditional dnaA mutants of Escherichia coli, only plasmid pSC101 has been shown to have a dnaA requirement. Experiments with dnaA null mutants of E. coli, presented here, show that dnaA plays a critical and direct role in the replication of miniplasmids derived from P1 and F as it does in the initiation of bacterial replication. Evidence is also presented for the existence of a dnaA-independent secondary replicon of P1 that is able to drive bacterial chromosome replication but is inadequate to support the maintenance of P1 as a plasmid in E. coli.

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Selected References

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  1. Abeles A. L., Snyder K. M., Chattoraj D. K. P1 plasmid replication: replicon structure. J Mol Biol. 1984 Mar 5;173(3):307–324. doi: 10.1016/0022-2836(84)90123-2. [DOI] [PubMed] [Google Scholar]
  2. Atlung T., Clausen E. S., Hansen F. G. Autoregulation of the dnaA gene of Escherichia coli K12. Mol Gen Genet. 1985;200(3):442–450. doi: 10.1007/BF00425729. [DOI] [PubMed] [Google Scholar]
  3. Austin S., Abeles A. Partition of unit-copy miniplasmids to daughter cells. I. P1 and F miniplasmids contain discrete, interchangeable sequences sufficient to promote equipartition. J Mol Biol. 1983 Sep 15;169(2):353–372. doi: 10.1016/s0022-2836(83)80055-2. [DOI] [PubMed] [Google Scholar]
  4. Austin S., Hart F., Abeles A., Sternberg N. Genetic and physical map of a P1 miniplasmid. J Bacteriol. 1982 Oct;152(1):63–71. doi: 10.1128/jb.152.1.63-71.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Braun R. E., O'Day K., Wright A. Autoregulation of the DNA replication gene dnaA in E. coli K-12. Cell. 1985 Jan;40(1):159–169. doi: 10.1016/0092-8674(85)90319-8. [DOI] [PubMed] [Google Scholar]
  6. Chandler M., Silver L., Caro L. Suppression of an Escherichia coli dnaA mutation by the integrated R factor R100.1: origin of chromosome replication during exponential growth. J Bacteriol. 1977 Aug;131(2):421–430. doi: 10.1128/jb.131.2.421-430.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chattoraj D. K., Snyder K. M., Abeles A. L. P1 plasmid replication: multiple functions of RepA protein at the origin. Proc Natl Acad Sci U S A. 1985 May;82(9):2588–2592. doi: 10.1073/pnas.82.9.2588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chattoraj D., Cordes K., Abeles A. Plasmid P1 replication: negative control by repeated DNA sequences. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6456–6460. doi: 10.1073/pnas.81.20.6456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chesney R. H., Scott J. R., Vapnek D. Integration of the plasmid prophages P1 and P7 into the chromosome of Escherichia coli. J Mol Biol. 1979 May 15;130(2):161–173. doi: 10.1016/0022-2836(79)90424-8. [DOI] [PubMed] [Google Scholar]
  10. Churchward G., Linder P., Caro L. The nucleotide sequence of replication and maintenance functions encoded by plasmid pSC101. Nucleic Acids Res. 1983 Aug 25;11(16):5645–5659. doi: 10.1093/nar/11.16.5645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Datta N., Barth P. T. Hfr formation by I pilus-determining plasmids in Escherichia coli K-12. J Bacteriol. 1976 Mar;125(3):811–817. doi: 10.1128/jb.125.3.811-817.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Donoghue D. J., Sharp P. A. Construction of a hybrid bacteriophage-plasmid recombinant DNA vector. J Bacteriol. 1978 Dec;136(3):1192–1196. doi: 10.1128/jb.136.3.1192-1196.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Felton J., Wright A. Plasmid pSC101 replication in integratively suppressed cells requires dnaA function. Mol Gen Genet. 1979 Sep;175(2):231–233. doi: 10.1007/BF00425541. [DOI] [PubMed] [Google Scholar]
  14. Frey J., Chandler M., Caro L. The effects of an Escherichia coli dnaAts mutation on the replication of the plasmids colE1 pSC101, R100.1 and RTF-TC. Mol Gen Genet. 1979 Jul 13;174(2):117–126. doi: 10.1007/BF00268349. [DOI] [PubMed] [Google Scholar]
  15. Fuller R. S., Funnell B. E., Kornberg A. The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell. 1984 Oct;38(3):889–900. doi: 10.1016/0092-8674(84)90284-8. [DOI] [PubMed] [Google Scholar]
  16. Fuller R. S., Kaguni J. M., Kornberg A. Enzymatic replication of the origin of the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7370–7374. doi: 10.1073/pnas.78.12.7370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hansen E. B., Atlung T., Hansen F. G., Skovgaard O., von Meyenburg K. Fine structure genetic map and complementation analysis of mutations in the dnaA gene of Escherichia coli. Mol Gen Genet. 1984;196(3):387–396. doi: 10.1007/BF00436184. [DOI] [PubMed] [Google Scholar]
  18. Hansen F. G., Rasmussen K. V. Regulation of the dnaA product in Escherichia coli. Mol Gen Genet. 1977 Oct 20;155(2):219–225. doi: 10.1007/BF00393163. [DOI] [PubMed] [Google Scholar]
  19. Hansen F. G., von Meyenburg K. Characterization of the dnaA, gyrB and other genes in the dnaA region of the Escherichia coli chromosome on specialized transducing phages lambda tna. Mol Gen Genet. 1979 Sep;175(2):135–144. doi: 10.1007/BF00425529. [DOI] [PubMed] [Google Scholar]
  20. Hasunuma K., Sekiguchi M. Replication of plasmid pSC101 in Escherichia coli K12: requirement for dnaA function. Mol Gen Genet. 1977 Sep 9;154(3):225–230. doi: 10.1007/BF00571277. [DOI] [PubMed] [Google Scholar]
  21. Hirota Y., Mordoh J., Jacob F. On the process of cellular division in Escherichia coli. 3. Thermosensitive mutants of Escherichia coli altered in the process of DNA initiation. J Mol Biol. 1970 Nov 14;53(3):369–387. doi: 10.1016/0022-2836(70)90072-0. [DOI] [PubMed] [Google Scholar]
  22. Hooper I., Egan J. B. Coliphage 186 infection requires host initiation functions dnaA and dnaC. J Virol. 1981 Nov;40(2):599–601. doi: 10.1128/jvi.40.2.599-601.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Horiuchi T., Maki H., Sekiguchi M. RNase H-defective mutants of Escherichia coli: a possible discriminatory role of RNase H in initiation of DNA replication. Mol Gen Genet. 1984;195(1-2):17–22. doi: 10.1007/BF00332717. [DOI] [PubMed] [Google Scholar]
  24. KONDO E., MITSUHASHI S. DRUG RESISTANCE OF ENTERIC BACTERIA. IV. ACTIVE TRANSDUCING BACTERIOPHAGE P1 CM PRODUCED BY THE COMBINATION OF R FACTOR WITH BACTERIOPHAGE P1. J Bacteriol. 1964 Nov;88:1266–1276. doi: 10.1128/jb.88.5.1266-1276.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kamio Y., Tabuchi A., Itoh Y., Katagiri H., Terawaki Y. Complete nucleotide sequence of mini-Rts1 and its copy mutant. J Bacteriol. 1984 Apr;158(1):307–312. doi: 10.1128/jb.158.1.307-312.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Koppes L., Nordström K. Insertion of an R1 plasmid into the origin of replication of the E. coli chromosome: random timing of replication of the hybrid chromosome. Cell. 1986 Jan 17;44(1):117–124. doi: 10.1016/0092-8674(86)90490-3. [DOI] [PubMed] [Google Scholar]
  27. Lindahl G., Hirota Y., Jacob F. On the process of cellular division in Escherichia coli: replication of the bacterial chromosome under control of prophage P2. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2407–2411. doi: 10.1073/pnas.68.10.2407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lindahl G., Lindahl T. Initiation of DNA replication in Escherichia coli: RNase H-deficient mutants do not require the dnaA function. Mol Gen Genet. 1984;196(2):283–289. doi: 10.1007/BF00328061. [DOI] [PubMed] [Google Scholar]
  29. Linder P., Churchward G., Xia G. X., Yu Y. Y., Caro L. An essential replication gene, repA, of plasmid pSC101 is autoregulated. J Mol Biol. 1985 Feb 5;181(3):383–393. doi: 10.1016/0022-2836(85)90227-x. [DOI] [PubMed] [Google Scholar]
  30. Louarn J. M., Bouché J. P., Legendre F., Louarn J., Patte J. Characterization and properties of very large inversions of the E. coli chromosome along the origin-to-terminus axis. Mol Gen Genet. 1985;201(3):467–476. doi: 10.1007/BF00331341. [DOI] [PubMed] [Google Scholar]
  31. Louarn J., Bouché J. P., Patte J., Louarn J. M. Genetic inactivation of topoisomerase I suppresses a defect in initiation of chromosome replication in Escherichia coli. Mol Gen Genet. 1984;195(1-2):170–174. doi: 10.1007/BF00332741. [DOI] [PubMed] [Google Scholar]
  32. MONOD J., COHEN-BAZIRE G., COHN M. Sur la biosynthèse de la beta-galactosidase (lactase) chez Escherichia coli; la spécificité de l'induction. Biochim Biophys Acta. 1951 Nov;7(4):585–599. doi: 10.1016/0006-3002(51)90072-8. [DOI] [PubMed] [Google Scholar]
  33. Masai H., Kaziro Y., Arai K. Definition of oriR, the minimum DNA segment essential for initiation of R1 plasmid replication in vitro. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6814–6818. doi: 10.1073/pnas.80.22.6814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Matsui M., Oka A., Takanami M., Yasuda S., Hirota Y. Sites of dnaA protein-binding in the replication origin of the Escherichia coli K-12 chromosome. J Mol Biol. 1985 Aug 5;184(3):529–533. doi: 10.1016/0022-2836(85)90299-2. [DOI] [PubMed] [Google Scholar]
  35. Molin S., Nordström K. Control of plasmid R1 replication: functions involved in replication, copy number control, incompatibility, and switch-off of replication. J Bacteriol. 1980 Jan;141(1):111–120. doi: 10.1128/jb.141.1.111-120.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Moody E. E., Runge R. The integration of autonomous transmissible plasmids into the chromosome of Escherichia coli K12. Genet Res. 1972 Apr;19(2):181–186. doi: 10.1017/s0016672300014427. [DOI] [PubMed] [Google Scholar]
  37. Moriya S., Ogasawara N., Yoshikawa H. Structure and function of the region of the replication origin of the Bacillus subtilis chromosome. III. Nucleotide sequence of some 10,000 base pairs in the origin region. Nucleic Acids Res. 1985 Apr 11;13(7):2251–2265. doi: 10.1093/nar/13.7.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Murotsu T., Tsutsui H., Matsubara K. Identification of the minimal essential region for the replication origin of miniF plasmid. Mol Gen Genet. 1984;196(2):373–378. doi: 10.1007/BF00328075. [DOI] [PubMed] [Google Scholar]
  39. Nishimura Y., Caro L., Berg C. M., Hirota Y. Chromosome replication in Escherichia coli. IV. Control of chromosome replication and cell division by an integrated episome. J Mol Biol. 1971 Feb 14;55(3):441–456. doi: 10.1016/0022-2836(71)90328-7. [DOI] [PubMed] [Google Scholar]
  40. Ogawa T., Pickett G. G., Kogoma T., Kornberg A. RNase H confers specificity in the dnaA-dependent initiation of replication at the unique origin of the Escherichia coli chromosome in vivo and in vitro. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1040–1044. doi: 10.1073/pnas.81.4.1040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ryder T. B., Davidson D. B., Rosen J. I., Ohtsubo E., Ohtsubo H. Analysis of plasmid genome evolution based on nucleotide-sequence comparison of two related plasmids of Escherichia coli. Gene. 1982 Mar;17(3):299–310. doi: 10.1016/0378-1119(82)90146-9. [DOI] [PubMed] [Google Scholar]
  42. Saadi S., Maas W. K., Bergquist P. L. RepFIC, a basic replicon of IncFI plasmids that has homology with a basic replicon of IncFII plasmids. Plasmid. 1984 Jul;12(1):61–64. doi: 10.1016/0147-619x(84)90067-2. [DOI] [PubMed] [Google Scholar]
  43. Saedler H., Heiss B. Multiple copies of the insertion-DNA sequences IS1 and IS2 in the chromosome of E. coli K-12. Mol Gen Genet. 1973 May 9;122(3):267–277. doi: 10.1007/BF00278602. [DOI] [PubMed] [Google Scholar]
  44. Sako T., Sakakibara Y. Coordinate expression of Escherichia coli dnaA and dnaN genes. Mol Gen Genet. 1980;179(3):521–526. doi: 10.1007/BF00271741. [DOI] [PubMed] [Google Scholar]
  45. Selzer G., Som T., Itoh T., Tomizawa J. The origin of replication of plasmid p15A and comparative studies on the nucleotide sequences around the origin of related plasmids. Cell. 1983 Jan;32(1):119–129. doi: 10.1016/0092-8674(83)90502-0. [DOI] [PubMed] [Google Scholar]
  46. Sotomura M., Yoshikawa M. Reinitiation of chromosome replication in the presence of chloramphenicol under an integratively suppressed state by R6K. J Bacteriol. 1975 May;122(2):623–628. doi: 10.1128/jb.122.2.623-628.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sternberg N., Austin S. Isolation and characterization of P1 minireplicons, lambda-P1:5R and lambda-P1:5L. J Bacteriol. 1983 Feb;153(2):800–812. doi: 10.1128/jb.153.2.800-812.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sternberg N., Hamilton D., Hoess R. Bacteriophage P1 site-specific recombination. II. Recombination between loxP and the bacterial chromosome. J Mol Biol. 1981 Aug 25;150(4):487–507. doi: 10.1016/0022-2836(81)90376-4. [DOI] [PubMed] [Google Scholar]
  49. Sternberg N., Hoess R. The molecular genetics of bacteriophage P1. Annu Rev Genet. 1983;17:123–154. doi: 10.1146/annurev.ge.17.120183.001011. [DOI] [PubMed] [Google Scholar]
  50. Søgaard-Andersen L., Rokeach L. A., Molin S. Regulated expression of a gene important for replication of plasmid F in E. coli. EMBO J. 1984 Feb;3(2):257–262. doi: 10.1002/j.1460-2075.1984.tb01794.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Tsutsui H., Fujiyama A., Murotsu T., Matsubara K. Role of nine repeating sequences of the mini-F genome for expression of F-specific incompatibility phenotype and copy number control. J Bacteriol. 1983 Jul;155(1):337–344. doi: 10.1128/jb.155.1.337-344.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wilson G. G., Young K. Y., Edlin G. J., Konigsberg W. High-frequency generalised transduction by bacteriophage T4. Nature. 1979 Jul 5;280(5717):80–82. doi: 10.1038/280080a0. [DOI] [PubMed] [Google Scholar]
  53. Yamaguchi K., Tomizawa J. Establishment of Escherichia coli cells with an integrated high copy number plasmid. Mol Gen Genet. 1980;178(3):525–533. doi: 10.1007/BF00337857. [DOI] [PubMed] [Google Scholar]
  54. Yamaguchi K., Yamaguchi M. The replication origin of pSC101: the nucleotide sequence and replication functions of the ori region. Gene. 1984 Jul-Aug;29(1-2):211–219. doi: 10.1016/0378-1119(84)90181-1. [DOI] [PubMed] [Google Scholar]
  55. Yarmolinsky M. B., Stevens E. Replication-control functions block the induction of an SOS response by a damaged P1 bacteriophage. Mol Gen Genet. 1983;192(1-2):140–148. doi: 10.1007/BF00327659. [DOI] [PubMed] [Google Scholar]
  56. Yoshimoto H., Yoshikawa M. Chromosome-plasmid interaction in Escherichia coli K-12 carrying a thermosensitive plasmid, Rts1, in autonomous and in integrated states. J Bacteriol. 1975 Nov;124(2):661–667. doi: 10.1128/jb.124.2.661-667.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Zyskind J. W., Cleary J. M., Brusilow W. S., Harding N. E., Smith D. W. Chromosomal replication origin from the marine bacterium Vibrio harveyi functions in Escherichia coli: oriC consensus sequence. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1164–1168. doi: 10.1073/pnas.80.5.1164. [DOI] [PMC free article] [PubMed] [Google Scholar]

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