Journal of Microbiology

The Microbiological Society of Korea (한국미생물학회)
권호 표지

Conserved Virulence Factors of Pseudomonas aeruginosa are Required for Killing Bacillus subtilis

  • Published : 2005.10.01
Download PDF
⟨ Previous Next ⟩

Abstract

The multi-host pathogen, Pseudomonas aeruginosa, possesses an extraordinary versatility which makes it capable of surviving the adverse conditions provided by environmental, host, and, presumably, competing microbial factors in its natural habitats. Here, we investigated the P. aeruginosa-Bacillus subtilis interaction in laboratory conditions and found that some P. aeruginosa strains can outcompete B. subtilis in mixed planktonic cultures. This is accompanied by the loss of B. subtilis viability. The bactericidal activity of P. aeruginosa is measured on B. subtilis plate cultures. The bactericidal activity is attenuated in pqsA, mvfR, lasR, pilB, gacA, dsbA, rpoS, and phnAB mutants. These results suggest that P. aeruginosa utilizes a subset of conserved virulence pathways in order to survive the conditions provided by its bacterial neighbors.

Keywords

References

  1. Boles, B.R., M. Thoendel, and P.K. Singh. 2004. Self-generated diversity produces 'insurance effects' in biofilm communities. Proc. Natl. Acad. Sci. USA. 101, 16630-16635
  2. Cao, H., G. Krishnan, B. Goumnerov, J. Tsongalis, R. Tompkins, and L.G. Rahme. 2001. A quorum sensing-associated virulence gene of Pseudomonas aeruginosa encodes a LysR-like transcription regulator with a unique self-regulatory mechanism. Proc. Natl. Acad. Sci. USA. 98, 14613-14618
  3. Cosson, P., L. Zulianello, O. Join-Lambert, F. Faurisson, L. Gebbie, M. Benghezal, C. van Delden, L.K. Curty, and T. Kohler. 2002. Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J. Bacteriol. 184, 3027-3033 https://doi.org/10.1128/JB.184.11.3027-3033.2002
  4. Costerton, J.W., Z. Lewandowski, D.E. Caldwell, D.R. Korber, and H.M. Lappin-Scott. 1995. Microbial biofilms. Ann. Rev. Microbiol. 49, 711-745 https://doi.org/10.1146/annurev.mi.49.100195.003431
  5. D'Argenio, D.A., L.A. Gallagher, C.A. Berg, and C. Manoil. 2001. Drosophila as a model host for Pseudomonas aeruginosa infection. J. Bacteriol. 183, 1466-1471 https://doi.org/10.1128/JB.183.4.1466-1471.2001
  6. D'Argenio, D.A., M.W. Calfee, P.B. Rainey, and E.C. Pesci. 2002. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184, 6481-6489 https://doi.org/10.1128/JB.184.23.6481-6489.2002
  7. Deretic, V., M.J. Schurr, and H. Yu. 1995. Pseudomonas aeruginosa, mucoidy and the chronic infection phenotype in cystic fibrosis. Trends Microbiol. 3, 351-356 https://doi.org/10.1016/S0966-842X(00)88974-X
  8. Deziel, E., F. Lepine, S. Milot, J. He, M.N. Mindrinos, R.G. Tompkins, and L.G. Rahme. 2004. Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4- hydroxy-2-heptylquinoline in cell-to-cell communication. Proc. Natl. Acad. Sci. USA. 101, 1339-1344
  9. Deziel, E., S. Gopalan, A.P. Tampakaki, F. Lepine, K.E. Padfield, M. Saucier, G. Xiao, and L.G. Rahme. 2005. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol. Microbiol. 55, 998-1014 https://doi.org/10.1111/j.1365-2958.2004.04448.x
  10. Deziel, E., Y. Comeau, and R. Villemur. 2001. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J. Bacteriol. 183, 1195-1204 https://doi.org/10.1128/JB.183.4.1195-1204.2001
  11. Dong, Y.H., A.R. Gusti, Q. Zhang, J.L. Xu, and L.H. Zhang. 2002. Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68, 1754-1749 https://doi.org/10.1128/AEM.68.4.1754-1759.2002
  12. Dong, Y.H., L.H. Wang, J.L. Xu, H.B. Zhang, X.F. Zhang, and L.H. Zhang. 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411, 813- 817 https://doi.org/10.1038/35081101
  13. Essar, D.W., L. Eberly, A. Hadero, and I.P. Crawford. 1990. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J. Bacteriol. 172, 884-900
  14. Frost, L.S. and W. Paranchych. 1977. Composition and molecular weight of pili purified from Pseudomonas aeruginosa K. J. Bacteriol. 131, 259-269
  15. Gallagher, L.A., S.L. McKnight, M.S. Kuznetsova, E.C. Pesci, and C. Manoil. 2002. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J. Bacteriol. 184, 6472- 6480 https://doi.org/10.1128/JB.184.23.6472-6480.2002
  16. Gang, R.K., R.L. Bang, S.C. Sanyal, E. Mokaddas, and A.R. Lari. 1999. Pseudomonas aeruginosa septicaemia in burns. Burns 25, 611-616 https://doi.org/10.1016/S0305-4179(99)00042-X
  17. Hacker, J. and J.B. Kaper. 2000. Pathogenicity islands and the evolution of microbes. Ann. Rev. Microbiol. 54, 641-679 https://doi.org/10.1146/annurev.micro.54.1.641
  18. HauBler, S. 2004. Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Environ. Microbiol. 6, 546-551. https://doi.org/10.1111/j.1462-2920.2004.00618.x
  19. Hentzer, M., H. Wu, J.B. Andersen, K. Riedel, T.B. Rasmussen, N. Bagge, N. Kumar, M.A. Schembri, Z. Song, P. Kristoffersen, M. Manefield, J.W. Costerton, S. Molin, L. Eberl, P. Steinberg, S. Kjelleberg, N. Hoiby, and M. Givskov. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22, 3803-3815 https://doi.org/10.1093/emboj/cdg366
  20. Heo, Y.-J., K.S. Ko, J.-H. Song, and Y.-H. Cho. 2005. Profiling pyocins and competitive growth advantages in various Pseudomonas aeruginosa strains. J. Microbiol. Biotech. in press
  21. Hoang, T.T., R.R. Karkhoff-Schweizer, A.J. Kutchma, and H.P. Schweizer HP. 1988. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene. 212, 77-86 https://doi.org/10.1016/S0378-1119(98)00130-9
  22. Hogan, D.A. and R. Kolter. 2002. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296, 2229-2232 https://doi.org/10.1126/science.1070784
  23. Hogan, D.A., A. Vik, and R. Kolter. 2004. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol. 54, 1212-1223 https://doi.org/10.1111/j.1365-2958.2004.04349.x
  24. Holloway, B.W. 1969. Genetics of Pseudomonas. Bacteriol. Rev. 33, 419-443
  25. Jander, G., L.G. Rahme, and F.M. Ausubel. 2000. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182, 3843-3845 https://doi.org/10.1128/JB.182.13.3843-3845.2000
  26. Jin, U.-H., S.-H. Cho, M.-G. Kim, S.-D. Ha, K.-S. Kim, K-H. Lee, K.-Y. Kim, D.H. Chung, Y.-C. Lee, and C.-H. Kim. 2004. PCR method based on the ogdH gene for the detection of Salmonella spp. from chicken meat samples. J. Microbiol. 42, 216-222
  27. Kim, S.-H. 2004. Roles of virulence factors in the interaction between Pseudomonas aeruginosa and Bacillus subtilis. M.S. thesis. Sogang University, Seoul, Korea
  28. Lau, G.W., B.C. Goumnerov, C.L. Walendziewicz, J. Hewitson, W. Xiao, S. Mahajan-Miklos, R.G. Tompkins, L.A. Perkins, and L.G. Rahme. 2003. The Drosophila melanogaster Toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect. Immun. 71, 4059-4066 https://doi.org/10.1128/IAI.71.7.4059-4066.2003
  29. Lau, G.W., D.J. Hassett, H. Ran, and F. Kong. 2004. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol. Med. 10, 599-606 https://doi.org/10.1016/j.molmed.2004.10.002
  30. Lee, J.-S., S.-H. Kim, and Y.-H. Cho. 2004. Dithiothreitol attenuates the pathogenic interaction between Pseudomonas aeruginosa and Drosophila melanogaster. J. Microbiol. Biotech. 14, 367-372
  31. Lee, J.-S., Y.-J. Heo, J.K. Lee, and Y.-H. Cho. 2005. KatA, the major catalase, is critical for osmoprotection and virulence in Pseudomonas aeruginosa PA14. Infect. Immun. 73, 4399-4403 https://doi.org/10.1128/IAI.73.7.4399-4403.2005
  32. Lee, Y.K., K.-K. Kwon, K.H. Cho, H.W. Kim, J.H. Park, and H.K. Lee. 2003. Culture and identification of bacteria from marine biofilms. J. Microbiol. 41, 183-188
  33. Lepine, F., E. Deziel, S. Milot, and L.G. Rahme. 2003. A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseudomonas aeruginosa cultures. Biochim. Biophys. Acta. 1622, 36-41 https://doi.org/10.1016/S0304-4165(03)00103-X
  34. Machan, Z.A., G.W. Taylorm T.L. Pitt, P.J. Cole, and R. Wilson. 1992. 2-Heptyl-4-hydroxyquinoline N-oxide, an antistaphylococcal agent produced by Pseudomonas aeruginosa. J. Antimicrob. Chemother. 30, 615-623 https://doi.org/10.1093/jac/30.5.615
  35. Mahajan-Miklos, S., M.W. Tan, L.G. Rahme, and F.M. Ausubel. 1999. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96, 47-56 https://doi.org/10.1016/S0092-8674(00)80958-7
  36. Mashburn, L.M., A.M. Jett, D.R. Akins, and M. Whiteley. 2005. Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J. Bacteriol. 187, 554- 566 https://doi.org/10.1128/JB.187.2.554-566.2005
  37. Ornston, L.N. and D. Parke. 1977. The evolution of induction mechanisms in bacteria: insights derived from the study of the $\beta$-ketoadipate pathway. Curr. Top. Cell Regul. 12, 209-62
  38. Pukatzki, S., R.H. Kessin, and J.J. Mekalanos. 2002. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc. Natl. Acad. Sci. USA. 99, 3159-3164
  39. Rahme, L.G., E.J. Stevens, S.F. Wolfort, J. Shao, R.G. Tompkins, and F.M. Ausubel. 1995. Common virulence factors for bacterial pathogenicity in plants and animals. Science 268, 1899- 1902 https://doi.org/10.1126/science.7604262
  40. Rahme, L.G., F.M. Ausubel, H. Cao, E. Drenkard, B.C. Goumnerov, G.W. Lau, S. Mahajan-Miklos, J. Plotnikova, M.W. Tan, J. Tsongalis, C.L. Walendziewicz, and Tompkins, R.G. 2000. Plants and animals share functionally common bacterial virulence factors. Proc. Natl. Acad. Sci. USA. 97, 8815-8821
  41. Ramos, J.L., E. Duque, P. Godoy, and A. Segura. 1998. Efflux pumps involved in toluene tolerance in Pseudomonas putida DOT-T1E. J. Bacteriol. 180, 3323-3329
  42. Sambrook, J. and D.W. Russel. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, New York
  43. Schuster, M., C.P. Lostroh, T. Ogi, and E.P. Greenberg. 2003. Idetification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185, 2066-2079 https://doi.org/10.1128/JB.185.7.2066-2079.2003
  44. Shin, I., H.-B. Ryu, H.-S. Yim, and S.-O. Kang. 2005. Cytochrome $c_{550}$ is related to inhibition of sporulation in Bacillus subtilis. J. Microbiol. 43, 244-250
  45. Simon, R., U. Priefer, and A. Puhler. 1983. A broad-host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Biotechnology 1, 784-791 https://doi.org/10.1038/nbt1183-784
  46. Tan, M.-W, L.G. Rahme, J.A. Sternberg, R.G. Tompkins, and F.M. Ausubel. 1999. Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc. Natl. Acad. Sci. USA. 96, 2408-2413
  47. Van Delden, C. and B.H. Iglewski. 1998. Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg. Infect. Dis. 4, 551-560 https://doi.org/10.3201/eid0404.980405
  48. Wade, D.S., M.W. Calfee, E.R. Rocha, E.A. Ling, E. Engstrom, J.P. Coleman, and E.C. Pesci. 2005. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J. Bacteriol. 187, 4372-4380 https://doi.org/10.1128/JB.187.13.4372-4380.2005