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Histone-like protein H-NS as a negative regulator of quorum sensing systems in gram-negative bacteria

  • Genetics of Microorganisms
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Abstract

The effects of histone-like protein H-NS on transcription of promoters of the Quorum Sensing regulated operons from marine luminescent mesophilic bacterium Aliivibrio fischeri and psychrophilic Aliivibrio logei, as well as from pathogenic Pseudomonas aeruginosa, are studied. In the present work, the plasmids carrying DNA fragments with the promoters Pr1f (upstream of the luxICDABEG operon from A. fischeri), Pr1l (upstream of the luxCDABEG operon from A. logei), Pr2l (upstream of luxI gene from A. logei), PluxCf (upstream of luxC gene from A. fischeri), and PlasI (upstream of lasI gene from P. aerugenosa) are used. In these plasmids, promoter-operator regions are transcriptionally fused to the reporter genes cassette luxCDABE from Photorhabdus luminescens. Here we have shown that the transcription of the QS-regulated promoters in E. coli hns::kan cells increases 100 to 1000 times. Furthermore, transcription of the QS-regulated promoters in E. coli hns + cells increases 10 to 100 times in the cells transformed with the plasmid carrying gene ardA ColIb-P9 encoding DNA mimic antirestriction protein ArdA, inhibitor of the type I restriction-modification systems.

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References

  1. Waters, C. and Bassler, B., Quorum Sensing: cell-tocell communication in bacteria, Annu. Rev. Cell Dev. Biol., 2005, vol. 21, pp. 319–346. doi 10.1146/annurev. cellbio.21.012704.131001

    Article  CAS  PubMed  Google Scholar 

  2. Khmel, I.A. and Metlitskaya, A.Z., Quorum sensing regulation of gene expression: a promising target for drugs against bacterial pathogenicity, Mol. Biol. (Mos-cow), 2006, vol. 40, no. 2, pp. 169–182. doi 10.1134/S0026893306020014

    Article  CAS  Google Scholar 

  3. Li, Z. and Nair, S.K., Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals?, Protein Sci., 2012, vol. 21, pp. 1403–1417. doi 10.1002/pro.2132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Fuqua, W.C., Winans, S.C., and Greenberg, E.P., Quorum sensing in bacteria: the LuxR–LuxI family of cell density–responsive transcriptional regulators, J. Bacteriol., 1994, vol. 176, pp. 269–275.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Fuqua, W.C., Winans, S.C., and Greenberg, E.P., Census and consensus in bacterial ecosystems: the LuxR–LuxI family of quorum sensing transcriptional regulators, Annu. Rev. Microbiol., 1996, vol. 50, pp. 727–751. doi 10.1146/annurev.micro.50.1.727

    Article  CAS  PubMed  Google Scholar 

  6. Meighen, E.A. and Dunlap, P.V., Physiological, biochemical and genetic control of bacterial bioluminescence, Adv. Microb. Physiol., 1993, vol. 34, pp. 1–67.

    CAS  PubMed  Google Scholar 

  7. Ulitzur, S., Matin, A., Fraley, C., and Meighen, E., H-NS protein represses transcription of the lux systems of Vibrio fischeri and other luminous bacteria cloned into Escherichia coli, Curr. Microbiol., 1997, vol. 35, pp. 336–342.

    Article  CAS  PubMed  Google Scholar 

  8. Yamada, H., Yoshida, T., Tanaka, K., et al., Molecular analysis of the Escherichia coli hns gene encoding a DNA-binding protein, which preferentially recognizes curved DNA sequences, Mol. Gen. Genet., 1991, vol. 230, pp. 332–336.

    Article  CAS  PubMed  Google Scholar 

  9. Owen-Hughes, T.A., Pavitt, G.D., Santos, D.S., et al., The chromatin-associated protein H-NS interacts with curved DNA to influence DNA topology and gene expression, Cell, 1992, vol. 71, pp. 255–265. doi 10.1016/0092-8674(92)90354-F

    Article  CAS  PubMed  Google Scholar 

  10. Azam, T.A. and Ishichama, A., Twelve species of the nucleoid-associated protein from Escherichia coli: sequence recognition specificity and DNA binding affinity, J. Biol. Chem., 1999, vol. 274, pp. 33105–33113. doi 10.1074/jbc.274.46.33105

    Article  CAS  PubMed  Google Scholar 

  11. Ueguchi, C. and Mizuno, T., The Escherichia coli nucleoid protein H-NS functions directly as a transcriptional repressor, EMBO J., 1993, vol. 12, pp. 1039–1046. doi 10.1006/jmbi.1996.0566

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Atlung, T. and Ingmer, H., H-NS: a modulator of environmentally regulated gene expression, Mol. Microbiol., 1997, vol. 24, pp. 7–17. doi 10.1046/j.1365-2958.1997.3151679.x

    Article  CAS  PubMed  Google Scholar 

  13. Noom, M.C., Navarre, W.W., Oshima, T., et al., H-NS promotes looped domain formation in the bacterial chromosome, Curr. Biol., 2007, vol. 17, pp. R913–R914. doi 10.1016/j.cub.2007.09.005

    Article  CAS  PubMed  Google Scholar 

  14. Bouffartigues, E., Buckle, M., Badaut, C., et al., H-NS cooperative binding to high-affinity sites in a regulatory element results in transcriptional silencing, Nat. Struct. Mol. Biol., 2007, vol. 14, pp. 441–448. doi 10.1038/nsmb1233

    Article  CAS  PubMed  Google Scholar 

  15. Dorman, C.J., H-NS, the genome sentinel, Nat. Rev. Microbiol., 2007, vol. 5, pp. 157–161. doi 10.1038/nrmicro1598

    Article  CAS  PubMed  Google Scholar 

  16. Ali, S.S., Xia, B., Liu, J., and Navarre, W.W., Silencing of foreign DNA in bacteria, Curr. Opin. Microbiol., 2012, vol. 15, pp. 175–161.

    Article  CAS  PubMed  Google Scholar 

  17. Dorman, C.J., H-NS-like nucleotid-associated proteins, mobile genetic elements and horizontal gene transfer in bacteria, Plasmid, 2014, vol. 75, pp. 1–11. doi 10.1016/j.plasmid.2014.06.004

    Article  CAS  PubMed  Google Scholar 

  18. Purtov, Y.A., Glazunova, O.A., Antipov, S.S., et al., Promoter islands as a platform for interaction with nucleoid proteins and transcription factors, J. Bioinf. Comput. Biol., 2014, vol. 12, no. 2. doi 10.1142/S0219720014410066

  19. Zhu, J. and Winans, S.C., The quorum-sensing transcriptional regulator TraR requires its cognate signaling ligand for protein folding, protease resistance, and dimerization, Proc. Natl. Acad. Sci. U.S.A., 2001, vol. 98, pp. 1507–1512. doi 10.1073/pnas.98.4.1507

    Article  CAS  PubMed  Google Scholar 

  20. Manukhov, I.V., Khrul’mova, S.A., Baranova, A., and Zavilgelsky, G.B., Comparative analysis of the lux operons in Aliivibrio logei Kch1 (a Kamchatka isolate) and Aliivibrio salmonicida, J. Bacteriol., 2011, vol. 193, pp. 3998–4001. doi 10.1128/JB.05320-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Pearson, J.P., Pesei, E.C., and Iglewski, B.H., Role of P. aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes, J. Bacteriol., 1997, vol. 179, pp. 5756–5767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Smith, R.S. and Iglewski, B.H.P., P. aeruginosa quorum- sensing systems and virulence, Curr. Opin. Microbiol., 2003, vol. 6, pp. 56–60. doi 10.1016/S1369-5274(03)00008-0

    Article  CAS  PubMed  Google Scholar 

  23. Fomenko, D., Veselowskii, A., and Khmel, I.A., Regulation of microcin C51 operon expression: the role of global regulators of transcription, Res. Microbiol., 2001, vol. 152, pp. 469–479. doi 10.1016/S0923- 2508(01)01220-7

    Article  CAS  PubMed  Google Scholar 

  24. van Dyk, T.K. and Rosson, R.A. Photorhabdus luminescens luxCDABE promoter probe vectors, in Methods in Molecular Biology, Larossa, R.A., Ed., Totowa, NJ: Humana, 1998, vol. 102, pp. 85–95. doi 10.1385/0- 89603-520-4:85

    Google Scholar 

  25. Robin, S., Togashi, D., Ryder, A.G., and Wall, J.G., Trigger factor from psychrophilic bacterium Psychrobacter frigidicola is a monomeric chaperone, J. Bacteriol., 2009, vol. 191, pp. 1162–1619. doi 10.1128/JB.01137-08

    Article  CAS  PubMed  Google Scholar 

  26. Mel’kina, O.E., Manukhov, I.V., and Zavilgelsky, G.B., The C-terminal domain of the Vibrio fischeri transcription activator LuxR is not essential for degradation by Lon protease, Mol. Biol. (Moscow), 2010, vol. 44, no. 3, pp. 454–457. doi 10.1134/S0026893-310030143

    Article  Google Scholar 

  27. Manukhov, I.V., Kotova, V.Yu., and Zavilgelsky, G.B., Involvement of host factors in the regulation of the Vibrio fischeri lux operon in Escherichia coli cells, Mikrobiologiya, 2006, vol. 75. pp. 525–531.

    CAS  Google Scholar 

  28. Khrulnova, S.A., Baranova, A., Bazhenov, S.V., et al., Lux-operon of the marine psychrophilic bacteria Aliivibrio logei: a comparative analysis of the LuxR1/LuxR2 regulatory activity in Escherichia coli cells, Microbiology, 2016, vol. 162. pp 717–724. doi 10.1099/mic.0.000253

    Article  CAS  Google Scholar 

  29. Lindsay, A. and Ahmer, B.M.M., Effect of sdiA on biosensors of N-acylhomoserine-lactones, J. Bacteriol., 2005, vol. 187, pp. 5054–5058. doi 10.1128/JB. 187.14.5054-5058.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zavilgelskii, G.B., Kotova, V.Yu., and Rastorguev, S.M., Antimodification activity of the ArdA and Ocr proteins, Russ. J. Genet., 2011, vol. 47, no. 2, pp. 139–146. doi 10.1134/S1022795410081034

    Article  Google Scholar 

  31. Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, New York: Cold Spring Harbor Lab., 1989, 2nd ed.

  32. Belogurov, A.A., Yusiffov, T.N., Kotova, V.Yu., and Zavilgelsky, G.B., The novel gene(s) ARD of plasmid pKM101: alleviation of EcoK restriction, Mol. Gen. Genet., 1985, vol. 198, pp. 509–513.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. McMahon, S.A., Roberts, G.A., Johnson, K.A., et al., Extensive DNA mimicry by the ArdA anti-restriction protein and its role in the spread of antibiotic resistance, Nucleic Acids Res., 2009, vol. 37, pp. 4887–4897. doi 10.1093/nar/gkp478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Navarre, W.W., Porwollik, S., Wang, Y., et al., Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella, Science, 2006, vol. 313, pp. 236–238. doi 10.1126/science.1128794

    Article  CAS  PubMed  Google Scholar 

  36. Gordon, B.R., Li, Y., Cote, A., et al., Structural basis for recognition of AT-rich DNA by unrelated xenogenic silencing proteins, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, pp. 10690–10695. doi 10.1073/pnas. 1102544108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to O. E. Melkina.

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Original Russian Text © O.E. Melkina, I.I. Goryanin, G.B. Zavilgelsky, 2017, published in Genetika, 2017, Vol. 53, No. 2, pp. 165–172.

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Melkina, O.E., Goryanin, I.I. & Zavilgelsky, G.B. Histone-like protein H-NS as a negative regulator of quorum sensing systems in gram-negative bacteria. Russ J Genet 53, 187–194 (2017). https://doi.org/10.1134/S1022795417020065

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