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Proteolytic control of the antirestriction activity of Tn21, Tn5053, Tn5045, Tn501, and Tn402 non-conjugative transposons

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Abstract

Conjugative plasmids and conjugative transposons contain the genes, whose products specifically inhibit the type-I restriction-modification systems. Here, it is shown that non-conjugative transposons Tn21, Tn5053, Tn5045, Tn501, and Tn402 partially inhibit the restriction activity of the type-I restriction-modification endonuclease EcoKI (R2M2S1) into Escherichia coli K12 cells (phenomenon of restriction alleviation, RA). The antirestriction activity of the transposons is determined by the MerR and ArdD proteins. The antirestiction activity of transposons is absent in the clpX and clpP E. coli K12 mutants and is decreased in recA, recBC, and dnaQ (mutD) E. coli K12 mutants. The induction of the RA in response to the MerR and ArdD activities is consistent with the production of unmodified target sequences following DNA repair and DNA synthesis associated with recombination repair or replication errors. The RA effect is determined by the ClpXP-dependent degradation of the endonuclease activity R subunit of EcoKI (R2M2S1).

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References

  1. Zavilgelsky G.B. 2000. Antirestriction. Mol. Biol. (Moscow). 34, 724–732.

    Article  CAS  Google Scholar 

  2. Tock M.R., Dryden D.T.F. 2005. The biology of restriction and antirestriction. Curr. Opin. Microbiol. 8, 466–472.

    Article  CAS  PubMed  Google Scholar 

  3. Delver E.P., Kotova V.Yu., Zavilgelsky G.B., Belogurov A.A. 1991. Nucleotide sequence of the gene (ard) encoding the antirestriction protein of plasmid ColIb-P9. J. Bacteriol. 173, 5887–5892.

    PubMed Central  CAS  PubMed  Google Scholar 

  4. Chilley P.M., Wilkins B.M. 1995. Distribution of the ardA family of antirestriction genes on conjugative plasmids. Microbiology. 141, 2157–2164.

    Article  CAS  PubMed  Google Scholar 

  5. McMahon S.A., Roberts G.A., Jhonson K.A., Cooper L.P., Liu H., White J.H., Carter L.G., Singhvi B., Oke M., Walkinshaw M.D., Blakely G.W., Naismith J.H., Dryden D.T.F. 2009. Extensive DNA mimicry by the ArdA antirestriction protein and its role in the spread antibiotic resistance. Nucleic Acids Res. 37, 4887–4897.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Belogurov A.A., Delver E.P., Rodzevich O.V. 1993. Plasmid pKM101 encodes two nonhomologous antirestriction proteins (ArdA and ArdB) whose expression is controlled by homologous regulatory sequences. J. Bacteriol. 175, 4843–4850.

    PubMed Central  CAS  PubMed  Google Scholar 

  7. Serfiotis-Mitsa D., Herbert A.P., Roberts G.A., Soares D.C., White J.H., Blakely G.W., Uhrin D., Dryden D.T.F. 2010. The structure of the KlcA and ArdB proteins reveals a novel fold and antirestriction activity against type I DNA restriction systems in vivo but not in vitro. Nucleic Acids Res. 38, 1723–1737.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Balabanov V.P., Kotova V.Yu. Kholodii G.Ya., Mindlin S.Z., Zavilgelsky G.B. 2012. A novel gene, ardD, determines antirestriction activity of the non-conjugative transposon Tn5053 and is located antisense within the tniA gene. FEMS Microbiol. Lett. 337, 55–60.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Rastorguev S.M., Letuchaya T.A, Kholodii G.Ya., Mindlin S.Z., Nikiforov V.G., Zavilgelsky G.B. 1999. Antirestriction activity of metalloregulatory proteins ArsR and MerR. Mol. Biol. (Moscow). 33, 170–172.

    CAS  Google Scholar 

  10. Grinsted J., de la Cruz F., Altenbuchner J., Schmitt R. 1982. Complementation of transposition of tnpA mutants of Tn3, Tn21, Tn501, and Tn1721. Plasmid. 8, 276–286.

    Article  CAS  PubMed  Google Scholar 

  11. Kholodii G.Y., Yurieva O.V., Lomovskaya O.L., Gorlenko Z., Mindlin S.Z., Nikiforov V.G. 1995. Four genes, two ends, and a res region are involved in transposition of Tn5053: A paradigm for a novel family of transposons carrying either a mer operon or an integron. Mol. Microbiol. 17, 1189–1120.

    Article  CAS  PubMed  Google Scholar 

  12. Petrova M., Gorlenko Z., Mindlin S. 2011. Tn5045, a novel integron-containing antibiotic and chromate resistance transposon isolated from a permafrost bacterium. Res. Microbiol. 162, 337–345.

    Article  CAS  PubMed  Google Scholar 

  13. Sambrook J., Fritsch E.P., Maniatis T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press.

    Google Scholar 

  14. Kotova V.Yu., Belogurov A.A., Zavilgelsky G.B. 1988. Attenuation of type I restriction in the presence of IncI plasmids: General characterization and cloning of the ard gene. Mol. Biol. (Moscow). 22, 270–276.

    CAS  Google Scholar 

  15. Zavilgelsky G.B., Kotova V.Yu., Rastorguev S.M. 2011. Antimodification activity of the ArdA and Ocr proteins. Russ. J. Genet. 47, 159–167.

    Article  Google Scholar 

  16. Makovets S., Titheradge A.J.B., Murray N.E. 1998. ClpX and ClpP are essential for the efficient acquisition of genes specifying type IA and IB restriction systems. Mol. Microbiol. 28, 25–35.

    Article  CAS  PubMed  Google Scholar 

  17. Makovets S., Doronina V.A., Murray N.E. 1999. Regulation of endonuclease activity by proteolysis prevents breakage of unmodified bacterial chromosomes by type I restriction enzymes. Proc. Natl. Acad. Sci. U. S. A. 96, 9757–9662.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Doronina V.A., Murray N.E. 2001. The proteolytic control of restriction activity in Escherichia coli K-12. Mol. Microbiol. 39, 416–428.

    Article  CAS  PubMed  Google Scholar 

  19. Thoms B., Wackernagel W. 1982. UV-induced alleviation of λ restriction in Escherichia coli K12: Kinetics of induction and specificity of this SOS function. Mol. Gen. Genet. 186, 111–117.

    Article  CAS  PubMed  Google Scholar 

  20. Thoms B., Wackernagel W. 1984. Genetic control of damage-inducible restriction alleviation in Escherichia coli K12: An SOS function not repressed by lexA. Mol. Gen. Genet. 197, 297–303.

    Article  CAS  PubMed  Google Scholar 

  21. Kelleher J.E., Ralleigh E.A. 1994. Response to UV damage by four Escherichia coli K12 restriction systems. J. Bacteriol. 176, 5888–5896.

    PubMed Central  CAS  PubMed  Google Scholar 

  22. Belogurov A.A., Efimova E.P., Del’ver E.P., Zavilgelsky G.B. 1987. Attenuation of type I restriction in Escherichia coli: Effect of 2-aminopurine and 5-bromouracyl. Mol. Genet. Mikrobiol. Virusol. 11, 34–40.

    Google Scholar 

  23. Blakely G.W., Murray N.E. 2006. Control of the endonuclease activity of type I restriction-modification systems is required to maintain chromosome integrity following homologous recombination. Mol. Microbiol. 60, 883–893.

    Article  CAS  PubMed  Google Scholar 

  24. Efimova E.P., Delver E.P., Belogurov A.A. 1988. 2-Aminopurine and 5-bromouracil induce alleviation of type I restriction in Escherichia coli: Mismatches function as inducing signals?. Mol. Gen. Genet. 214, 317–320.

    Article  CAS  PubMed  Google Scholar 

  25. Belogurov A.A., Efimova E.P., Del’ver E.P., Zavilgelsky G.B. 1987. Attenuation of type I restriction in Escherichia coli: Effect of dam mutation. Mol. Genet. Mikrobiol. Virusol. 9, 10–16.

    Google Scholar 

  26. Chan A., Nagel R. 1997. Involvement of recA and recF in the induced precise excision of Tn10 in Escherichia coli. Mutat. Res. 381, 111–115.

    Article  CAS  PubMed  Google Scholar 

  27. Eichenbaum Z., Livneh Z. 1998. UV-light induces IS10 transposition in Escherichia coli. Genetics. 149, 1173–1181.

    PubMed Central  CAS  PubMed  Google Scholar 

  28. Aleshkin G.I., Kadzhaev K.V., Markov A.P. 1998. High and low UV-dose responses in SOS-induction of the precise excision of transposons Tn1, Tn5, and Tn10 in Escherichia coli. Mutation Res. 401, 179–191.

    Article  CAS  PubMed  Google Scholar 

  29. Shi Q., Parks A.R., Potter B.D., Safir I.J., Luo Y., Foster B.M., Peters J.E. 2008. DNA damage differentially activates regional chromosomal loci for T7 transposition in Escherichia coli. Genetics. 179, 1237–1250.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Correspondence to G. B. Zavilgelsky.

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Original Russian Text © G.B. Zavilgelsky, V.Yu. Kotova, O.E. Melkina, V.P. Balabanov, S.Z. Mindlin, 2015, published in Molekulyarnaya Biologiya, 2015, Vol. 49, No. 2, pp. 334–341.

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Zavilgelsky, G.B., Kotova, V.Y., Melkina, O.E. et al. Proteolytic control of the antirestriction activity of Tn21, Tn5053, Tn5045, Tn501, and Tn402 non-conjugative transposons. Mol Biol 49, 295–302 (2015). https://doi.org/10.1134/S0026893315020168

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