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. 1990 Jul;172(7):3600–3608. doi: 10.1128/jb.172.7.3600-3608.1990

Structural and functional similarities between the replication region of the Yersinia virulence plasmid and the RepFIIA replicons.

J C Vanooteghem 1, G R Cornelis 1
PMCID: PMC213333  PMID: 1694522

Abstract

We sequenced the minimum replication region of the virulence plasmid pYVe439-80 from a serogroup O:9 Yersinia enterocolitica. This sequence is 68% homologous on a 1,873-nucleotide stretch to the sequence of the RepFIIA replicon of the resistance plasmid R100. The sequence contains two open reading frames, repA and repB, encoding proteins of 33,478 and 9,568 daltons, respectively. The amino acid sequences of the two proteins are 77 and 55% identical, respectively, to proteins RepA1 and RepA2 of the R100 replicon. Analysis of minicells transformed with a copy number mutant demonstrated that the replication region of pYVe439-80 directs the synthesis of a 33-kilodalton protein. Disruption of repA, encoding this protein, abolished replication. Two regions of pYVe439-80 are 76 and 70% homologous, respectively, to the copy number control antisense RNA and to the origin of replication region of R100. A mutation introduced in the pYVe439-80 DNA corresponding to the R100 sequence encoding the copy number control antisense RNA resulted in an increase in copy number, indicating a functional homology between the two replicons.

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Selected References

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  1. Bakour R., Laroche Y., Cornelis G. Study of the incompatibility and replication of the 70-kb virulence plasmid of Yersinia. Plasmid. 1983 Nov;10(3):279–289. doi: 10.1016/0147-619x(83)90042-2. [DOI] [PubMed] [Google Scholar]
  2. Balligand G., Laroche Y., Cornelis G. Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination. Infect Immun. 1985 Jun;48(3):782–786. doi: 10.1128/iai.48.3.782-786.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ben-Gurion R., Shafferman A. Essential virulence determinants of different Yersinia species are carried on a common plasmid. Plasmid. 1981 Mar;5(2):183–187. doi: 10.1016/0147-619x(81)90019-6. [DOI] [PubMed] [Google Scholar]
  4. Biot T., Cornelis G. R. The replication, partition and yop regulation of the pYV plasmids are highly conserved in Yersinia enterocolitica and Y. pseudotuberculosis. J Gen Microbiol. 1988 Jun;134(6):1525–1534. doi: 10.1099/00221287-134-6-1525. [DOI] [PubMed] [Google Scholar]
  5. Bölin I., Forsberg A., Norlander L., Skurnik M., Wolf-Watz H. Identification and mapping of the temperature-inducible, plasmid-encoded proteins of Yersinia spp. Infect Immun. 1988 Feb;56(2):343–348. doi: 10.1128/iai.56.2.343-348.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bölin I., Portnoy D. A., Wolf-Watz H. Expression of the temperature-inducible outer membrane proteins of yersiniae. Infect Immun. 1985 Apr;48(1):234–240. doi: 10.1128/iai.48.1.234-240.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Caron J., Coffield L. M., Scott J. R. A plasmid-encoded regulatory gene, rns, required for expression of the CS1 and CS2 adhesins of enterotoxigenic Escherichia coli. Proc Natl Acad Sci U S A. 1989 Feb;86(3):963–967. doi: 10.1073/pnas.86.3.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chou P. Y., Fasman G. D. Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol Relat Areas Mol Biol. 1978;47:45–148. doi: 10.1002/9780470122921.ch2. [DOI] [PubMed] [Google Scholar]
  9. Claverie J. M. A common philosophy and FORTRAN 77 software package for implementing and searching sequence databases. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):397–407. doi: 10.1093/nar/12.1part1.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cornelis G. R., Biot T., Lambert de Rouvroit C., Michiels T., Mulder B., Sluiters C., Sory M. P., Van Bouchaute M., Vanooteghem J. C. The Yersinia yop regulon. Mol Microbiol. 1989 Oct;3(10):1455–1459. doi: 10.1111/j.1365-2958.1989.tb00129.x. [DOI] [PubMed] [Google Scholar]
  11. Cornelis G., Laroche Y., Balligand G., Sory M. P., Wauters G. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev Infect Dis. 1987 Jan-Feb;9(1):64–87. doi: 10.1093/clinids/9.1.64. [DOI] [PubMed] [Google Scholar]
  12. Cornelis G., Sluiters C., de Rouvroit C. L., Michiels T. Homology between virF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator. J Bacteriol. 1989 Jan;171(1):254–262. doi: 10.1128/jb.171.1.254-262.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cornelis G., Sory M. P., Laroche Y., Derclaye I. Genetic analysis of the plasmid region controlling virulence in Yersinia enterocolitica 0:9 by Mini-Mu insertions and lac gene fusions. Microb Pathog. 1986 Aug;1(4):349–359. doi: 10.1016/0882-4010(86)90067-7. [DOI] [PubMed] [Google Scholar]
  14. Cornelis G., Vanootegem J. C., Sluiters C. Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes. Microb Pathog. 1987 May;2(5):367–379. doi: 10.1016/0882-4010(87)90078-7. [DOI] [PubMed] [Google Scholar]
  15. Couturier M., Bex F., Bergquist P. L., Maas W. K. Identification and classification of bacterial plasmids. Microbiol Rev. 1988 Sep;52(3):375–395. doi: 10.1128/mr.52.3.375-395.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dale R. M., McClure B. A., Houchins J. P. A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA. Plasmid. 1985 Jan;13(1):31–40. doi: 10.1016/0147-619x(85)90053-8. [DOI] [PubMed] [Google Scholar]
  17. Dong X., Womble D. D., Luckow V. A., Rownd R. H. Regulation of transcription of the repA1 gene in the replication control region of IncFII plasmid NR1 by gene dosage of the repA2 transcription repressor protein. J Bacteriol. 1985 Feb;161(2):544–551. doi: 10.1128/jb.161.2.544-551.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gemski P., Lazere J. R., Casey T. Plasmid associated with pathogenicity and calcium dependency of Yersinia enterocolitica. Infect Immun. 1980 Feb;27(2):682–685. doi: 10.1128/iai.27.2.682-685.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gemski P., Lazere J. R., Casey T., Wohlhieter J. A. Presence of a virulence-associated plasmid in Yersinia pseudotuberculosis. Infect Immun. 1980 Jun;28(3):1044–1047. doi: 10.1128/iai.28.3.1044-1047.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Goguen J. D., Yother J., Straley S. C. Genetic analysis of the low calcium response in Yersinia pestis mu d1(Ap lac) insertion mutants. J Bacteriol. 1984 Dec;160(3):842–848. doi: 10.1128/jb.160.3.842-848.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Heesemann J., Gross U., Schmidt N., Laufs R. Immunochemical analysis of plasmid-encoded proteins released by enteropathogenic Yersinia sp. grown in calcium-deficient media. Infect Immun. 1986 Nov;54(2):561–567. doi: 10.1128/iai.54.2.561-567.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kingsbury D. T., Helinski D. R. Temperature-sensitive mutants for the replication of plasmids in Escherichia coli: requirement for deoxyribonucleic acid polymerase I in the replication of the plasmid ColE 1 . J Bacteriol. 1973 Jun;114(3):1116–1124. doi: 10.1128/jb.114.3.1116-1124.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kollek R., Oertel W., Goebel W. Isolation and characterization of the minimal fragment required for autonomous replication ("basic replicon") of a copy mutant (pKN102) of the antibiotic resistance factor R1. Mol Gen Genet. 1978 Jun 1;162(1):51–57. doi: 10.1007/BF00333850. [DOI] [PubMed] [Google Scholar]
  24. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  25. Laroche Y., van Bouchaute M., Cornelis G. A restriction map of virulence plasmid pVYE439-80 from a serogroup 9 Yersinia enterocolitica strain. Plasmid. 1984 Jul;12(1):67–70. doi: 10.1016/0147-619x(84)90069-6. [DOI] [PubMed] [Google Scholar]
  26. Light J., Molin S. The sites of action of the two copy number control functions of plasmid R1. Mol Gen Genet. 1982;187(3):486–493. doi: 10.1007/BF00332633. [DOI] [PubMed] [Google Scholar]
  27. Low B. Rapid mapping of conditional and auxotrophic mutations in Escherichia coli K-12. J Bacteriol. 1973 Feb;113(2):798–812. doi: 10.1128/jb.113.2.798-812.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Miller J., Manis J., Kline B., Bishop A. Nonintegrated plasmid-folded chromosome complexes: genetic studies on formation and possible relationship to plasmid replication. Plasmid. 1978 Jun;1(3):273–283. doi: 10.1016/0147-619x(78)90045-8. [DOI] [PubMed] [Google Scholar]
  29. Mulder B., Michiels T., Simonet M., Sory M. P., Cornelis G. Identification of additional virulence determinants on the pYV plasmid of Yersinia enterocolitica W227. Infect Immun. 1989 Aug;57(8):2534–2541. doi: 10.1128/iai.57.8.2534-2541.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. NAKAYA R., NAKAMURA A., MURATA Y. Resistance transfer agents in Shigella. Biochem Biophys Res Commun. 1960 Dec;3:654–659. doi: 10.1016/0006-291x(60)90081-4. [DOI] [PubMed] [Google Scholar]
  31. Ogura T., Hiraga S. Partition mechanism of F plasmid: two plasmid gene-encoded products and a cis-acting region are involved in partition. Cell. 1983 Feb;32(2):351–360. doi: 10.1016/0092-8674(83)90454-3. [DOI] [PubMed] [Google Scholar]
  32. Pohl P., Lintermans P., Bex F., Desmyter A., Dreze P., Fonteyne P. A., Couturier M. Propriétés phénotypiques et génotypiques de quatre plasmides de virulence de Salmonella typhimurium. Ann Inst Pasteur Microbiol. 1987 Sep-Oct;138(5):523–528. [PubMed] [Google Scholar]
  33. Portnoy D. A., Falkow S. Virulence-associated plasmids from Yersinia enterocolitica and Yersinia pestis. J Bacteriol. 1981 Dec;148(3):877–883. doi: 10.1128/jb.148.3.877-883.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Portnoy D. A., Moseley S. L., Falkow S. Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun. 1981 Feb;31(2):775–782. doi: 10.1128/iai.31.2.775-782.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Portnoy D. A., Wolf-Watz H., Bolin I., Beeder A. B., Falkow S. Characterization of common virulence plasmids in Yersinia species and their role in the expression of outer membrane proteins. Infect Immun. 1984 Jan;43(1):108–114. doi: 10.1128/iai.43.1.108-114.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Reeve J. N. Bacteriophage infection of minicells: a general method for identification of "in vivo" bacteriophage directed polypeptide biosynthesis. Mol Gen Genet. 1977 Dec 14;158(1):73–79. doi: 10.1007/BF00455121. [DOI] [PubMed] [Google Scholar]
  37. Rownd R. H., Womble D. D., Dong X. N., Luckow V. A., Wu R. P. Incompatibility and IncFII plasmid replication control. Basic Life Sci. 1985;30:335–354. doi: 10.1007/978-1-4613-2447-8_26. [DOI] [PubMed] [Google Scholar]
  38. Silva R. M., Saadi S., Maas W. K. A basic replicon of virulence-associated plasmids of Shigella spp. and enteroinvasive Escherichia coli is homologous with a basic replicon in plasmids of IncF groups. Infect Immun. 1988 Apr;56(4):836–842. doi: 10.1128/iai.56.4.836-842.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Straley S. C., Bowmer W. S. Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun. 1986 Feb;51(2):445–454. doi: 10.1128/iai.51.2.445-454.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Talmadge K., Gilberg W. Construction of plasmid vectors with unique PstI cloning sites in a signal sequence coding region. Gene. 1980 Dec;12(3-4):235–241. doi: 10.1016/0378-1119(80)90105-5. [DOI] [PubMed] [Google Scholar]
  42. Tang X. B., Womble D. D., Rownd R. H. DnaA protein is not essential for replication of IncFII plasmid NR1. J Bacteriol. 1989 Oct;171(10):5290–5295. doi: 10.1128/jb.171.10.5290-5295.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Taylor D. P., Cohen S. N. Structural and functional analysis of cloned DNA segments containing the replication and incompatibility regions of a miniplasmid derived from a copy number mutant of NR1. J Bacteriol. 1979 Jan;137(1):92–104. doi: 10.1128/jb.137.1.92-104.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Trinks K., Habermann P., Beyreuther K., Starlinger P., Ehring R. An IS4-encoded protein is synthesized in minicells. Mol Gen Genet. 1981;182(2):183–188. doi: 10.1007/BF00269656. [DOI] [PubMed] [Google Scholar]
  45. Wallace R. G., Lee N., Fowler A. V. The araC gene of Escherichia coli: transcriptional and translational start-points and complete nucleotide sequence. Gene. 1980 Dec;12(3-4):179–190. doi: 10.1016/0378-1119(80)90100-6. [DOI] [PubMed] [Google Scholar]
  46. Weber P. C., Palchaudhuri S. Incompatibility repressor in a RepA-like replicon of the IncFI plasmid ColV2-K94. J Bacteriol. 1986 Jun;166(3):1106–1112. doi: 10.1128/jb.166.3.1106-1112.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Womble D. D., Dong X., Wu R. P., Luckow V. A., Martinez A. F., Rownd R. H. IncFII plasmid incompatibility product and its target are both RNA transcripts. J Bacteriol. 1984 Oct;160(1):28–35. doi: 10.1128/jb.160.1.28-35.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Womble D. D., Rownd R. H. Genetic and physical map of plasmid NR1: comparison with other IncFII antibiotic resistance plasmids. Microbiol Rev. 1988 Dec;52(4):433–451. doi: 10.1128/mr.52.4.433-451.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Womble D. D., Sampathkumar P., Easton A. M., Luckow V. A., Rownd R. H. Transcription of the replication control region of the IncFII R-plasmid NR1 in vitro and in vivo. J Mol Biol. 1985 Feb 5;181(3):395–410. doi: 10.1016/0022-2836(85)90228-1. [DOI] [PubMed] [Google Scholar]
  50. Womble D. D., Taylor D. P., Rownd R. H. Method for obtaining more-accurate covalently closed circular plasmid-to-chromosome ratios from bacterial lysates by dye-buoyant density centrifugation. J Bacteriol. 1977 Apr;130(1):148–153. doi: 10.1128/jb.130.1.148-153.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yother J., Chamness T. W., Goguen J. D. Temperature-controlled plasmid regulon associated with low calcium response in Yersinia pestis. J Bacteriol. 1986 Feb;165(2):443–447. doi: 10.1128/jb.165.2.443-447.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Yother J., Goguen J. D. Isolation and characterization of Ca2+-blind mutants of Yersinia pestis. J Bacteriol. 1985 Nov;164(2):704–711. doi: 10.1128/jb.164.2.704-711.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Zuker M. Computer prediction of RNA structure. Methods Enzymol. 1989;180:262–288. doi: 10.1016/0076-6879(89)80106-5. [DOI] [PubMed] [Google Scholar]

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