DOI QR코드

DOI QR Code

Omics-Based Analysis of the luxS Mutation in a Clinical Isolate of Escherichia coli O157:H7 in Korea

  • Kim, Jong-Chul (Division of Enteric Bacterial Infections, Center for Infectious Diseases, National Institute of Health) ;
  • Yoon, Jang-Won (Advanced Human Resource and Research Group for Medical Science (BK21), Konkuk University School of Medicine) ;
  • Kim, Jong-Bae (Department of Biomedical Laboratory Science, College of Health Sciences, Yonsei University) ;
  • Oh, Kyung-Hwan (Division of Enteric Bacterial Infections, Center for Infectious Diseases, National Institute of Health) ;
  • Park, Mi-Sun (Division of Enteric Bacterial Infections, Center for Infectious Diseases, National Institute of Health) ;
  • Lee, Bok-Kwon (Division of Enteric Bacterial Infections, Center for Infectious Diseases, National Institute of Health) ;
  • Cho, Seung-Hak (Division of Enteric Bacterial Infections, Center for Infectious Diseases, National Institute of Health)
  • Published : 2010.02.28

Abstract

The purpose of this study was to investigate the relationship between the global regulatory mechanism known as quorum sensing and expression of virulence factors in Escherichia coli O157:87. A nonpolar luxS deletion was introduced into the chromosome of strain CI03J, a human clinical isolate from South Korea, to create the ${\Delta}luxS$ mutant strain ML03J. Phenotypic characterization of wild-type and mutant strains demonstrated that ML03J had no obvious growth or metabolic defects on 0.2% glucose LB medium, produced a functionally defective flagellum, and could not utilize sorbose; the biological significance of sorbose utilization is unknown. Omics-based analysis revealed the involvement of LuxS in the transcriptional activation of several flagella/chemotaxisrelated genes (flhD; fliA, C, D, S, Z; and cheA, Y, Z), repression of glutamate-dependent acid resistance genes (gadAB), and expression of virulence factors including Shiga toxin, hemolysin, and SepD within the LEE pathogenicity island.

Keywords

References

  1. Balaban, N. and R. P. Novick. 1995. Autocrine regulation of toxin synthesis by Staphylococcus aureus. Proc. Natl. Acad. Sci. U.S.A. 92: 1619-1623. https://doi.org/10.1073/pnas.92.5.1619
  2. Bansal, T., P. Jesudhasan, S. Pillai, T. K. Wood, and A. Jayaraman. 2008. Temporal regulation of enterohemorrhagic Escherichia coli virulence mediated by autoinducer-2. Appl. Microbiol. Biotechnol. 78: 811-819. https://doi.org/10.1007/s00253-008-1359-8
  3. Bhagwat, A. A. and M. Bhagwat. 2004. Comparative analysis of transcriptional regulatory elements of glutamate-dependent acid-resistance systems of Shigella flexneri and Escherichia coli O157:H7. FEMS Microbiol. Lett. 234: 139-147. https://doi.org/10.1111/j.1574-6968.2004.tb09525.x
  4. Chen, X., S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelczer, B. L. Bassler, and F. M. Hughson. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549. https://doi.org/10.1038/415545a
  5. Cherepanov, P. P. and W. Wackernagel. 1995. Gene disruption in Escherichia coli: $Tc^R$ and $Km^R$ cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14. https://doi.org/10.1016/0378-1119(95)00193-A
  6. Clarke, M. B. and V. Sperandio. 2005. Transcriptional autoregulation by quorum sensing Escherichia coli regulators B and C (QseBC) in enterohaemorrhagic E. coli (EHEC). Mol. Microbiol. 58: 441-455. https://doi.org/10.1111/j.1365-2958.2005.04819.x
  7. Clarke, M. B. and V. Sperandio. 2005. Transcriptional regulation of flhDC by QseBC and sigma (FliA) in enterohaemorrhagic Escherichia coli. Mol. Microbiol. 57: 1734-1749. https://doi.org/10.1111/j.1365-2958.2005.04792.x
  8. Datsenko, K. A. and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97: 6640-6645. https://doi.org/10.1073/pnas.120163297
  9. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95: 14863-14868. https://doi.org/10.1073/pnas.95.25.14863
  10. Frenzen, P. D. 2007. An online cost calculator for estimating the economic cost of illness due to Shiga toxin-producing E. coli (STEC) O157 infections. In U.S.D.A. (ed.). Economic Research Service, EBI-28.
  11. Gorg, A., C. Obermaier, G. Boguth, A. Harder, B. Scheibe, R. Wildgruber, and W. Weiss. 2000. The current state of twodimensional electrophoresis with immobilized pH gradients. Electrophoresis 21: 1037-1053. https://doi.org/10.1002/(SICI)1522-2683(20000401)21:6<1037::AID-ELPS1037>3.0.CO;2-V
  12. He, Y. W. and L. H. Zhang. 2008. Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol. Rev. 32: 842-857. https://doi.org/10.1111/j.1574-6976.2008.00120.x
  13. Huang, Y. J., T. Y. Tsai, and T. M. Pan. 2007. Physiological response and protein expression under acid stress of Escherichia coli O157:H7 TWC01 isolated from Taiwan. J. Agric. Food Chem. 55: 7182-7191. https://doi.org/10.1021/jf071014s
  14. Hughes, D. T. and V. Sperandio. 2008. Inter-kingdom signalling: Communication between bacteria and their hosts. Nat. Rev. Microbiol. 6: 111-120. https://doi.org/10.1038/nrmicro1836
  15. Jayaraman, A. and T. K. Wood. 2008. Bacterial quorum sensing: Signals, circuits, and implications for biofilms and disease. Annu. Rev. Biomed. Eng. 10: 145-167. https://doi.org/10.1146/annurev.bioeng.10.061807.160536
  16. Jeon, B., and K. Itoh. 2007. Production of Shiga toxin by a luxS mutant of Escherichia coli O157:H7 in vivo and in vitro. Microbiol. Immunol. 51: 391-396.
  17. Karmali, M. A., B. T. Steele, M. Petric, and C. Lim. 1983. Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet 1: 619-620.
  18. Kendall, M. M., D. A. Rasko, and V. Sperandio. 2007. Global effects of the cell-to-cell signaling molecules autoinducer-2, autoinducer-3, and epinephrine in a luxS mutant of enterohemorrhagic Escherichia coli. Infect. Immun. 75: 4875-4884. https://doi.org/10.1128/IAI.00550-07
  19. Kenny, B., A. Abe, M. Stein, and B. B. Finlay. 1997. Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect. Immun. 65: 2606-2612.
  20. Komoriya, K., N. Shibano, T. Higano, N. Azuma, S. Yamaguchi, and S. I. Aizawa. 1999. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol. Microbiol. 34: 767-779. https://doi.org/10.1046/j.1365-2958.1999.01639.x
  21. Lehmacher, A. and J. Bockemuhl. 2007. L-Sorbose utilization by virulent Escherichia coli and Shigella: Different metabolic adaptation of pathotypes. Int. J. Med. Microbiol. 297: 245-254. https://doi.org/10.1016/j.ijmm.2007.01.007
  22. Novick, R. P. and E. Geisinger. 2008. Quorum sensing in staphylococci. Annu. Rev. Genet. 42: 541-564. https://doi.org/10.1146/annurev.genet.42.110807.091640
  23. Oh, S., H. Im, E. Oh, J. Lee, J. Y. Khim, J. Mun, et al. 2004. Effects of benzo(a)pyrene on protein expression in Jurkat Tcells. Proteomics 4: 3514-3526. https://doi.org/10.1002/pmic.200400981
  24. Riley, L. W., R. S. Remis, S. D. Helgerson, H. B. McGee, J. G. Wells, B. R. Davis, et al. 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308: 681-685. https://doi.org/10.1056/NEJM198303243081203
  25. Senadheera, D. and D. G. Cvitkovitch. 2008. Quorum sensing and biofilm formation by Streptococcus mutans. Adv. Exp. Med. Biol. 631: 178-188. https://doi.org/10.1007/978-0-387-78885-2_12
  26. Soni, K., P. Jesudhasan, M. Cepeda, B. Williams, M. Hume, W. K. Russell, A. Jayaraman, and S. D. Pillai. 2007. Proteomic analysis to identify the role of LuxS/AI-2 mediated protein expression in Escherichia coli O157:H7. Foodborne Pathog. Dis. 4: 463-471. https://doi.org/10.1089/fpd.2007.0034
  27. Sperandio, V., J. L. Mellies, W. Nguyen, S. Shin, and J. B. Kaper. 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96: 15196-15201. https://doi.org/10.1073/pnas.96.26.15196
  28. Sperandio, V., A. G. Torres, J. A. Giron, and J. B. Kaper. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183: 5187-5197. https://doi.org/10.1128/JB.183.17.5187-5197.2001
  29. Sperandio, V., A. G. Torres, B. Jarvis, J. P. Nataro, and J. B. Kaper. 2003. Bacteria-host communication: The language of hormones. Proc. Natl. Acad. Sci. U.S.A. 100: 8951-8956. https://doi.org/10.1073/pnas.1537100100
  30. Sperandio, V., A. G. Torres, and J. B. Kaper. 2002. Quorum sensing Escherichia coli regulators B and C (QseBC): A novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol. Microbiol. 43: 809-821. https://doi.org/10.1046/j.1365-2958.2002.02803.x
  31. Surette, M. G., M. B. Miller, and B. L. Bassler. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: A new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. U.S.A. 96: 1639-1644. https://doi.org/10.1073/pnas.96.4.1639
  32. von Bodman, S. B., J. M. Willey, and S. P. Diggle. 2008. Cellcell communication in bacteria: United we stand. J. Bacteriol. 190: 4377-4391. https://doi.org/10.1128/JB.00486-08
  33. Walters, M., M. P. Sircili, and V. Sperandio. 2006. AI-3 synthesis is not dependent on luxS in Escherichia coli. J. Bacteriol. 188: 5668-5681. https://doi.org/10.1128/JB.00648-06
  34. Walters, M. and V. Sperandio. 2006. Quorum sensing in Escherichia coli and Salmonella. Int. J. Med. Microbiol. 296: 125-131.
  35. Wells, J. G., B. R. Davis, I. K. Wachsmuth, L. W. Riley, R. S. Remis, R. Sokolow, and G. K. Morris. 1983. Laboratory investigation of hemorrhagic colitis outbreaks associated with a rare Escherichia coli serotype. J. Clin. Microbiol. 18: 512-520.
  36. Yoon, J. W. and C. J. Hovde. 2008. All blood, no stool: Enterohemorrhagic Escherichia coli O157:H7 infection. J. Vet. Sci. 9: 219-231. https://doi.org/10.4142/jvs.2008.9.3.219

Cited by

  1. Distribution of Virulence Genes and Their Association of Serotypes in Pathogenic Escherichia coli Isolates From Diarrheal Patients in Korea vol.1, pp.1, 2010, https://doi.org/10.1016/j.phrp.2010.12.008
  2. Mutation design and strain background influence the phenotype of Escherichia coliluxS mutants vol.88, pp.5, 2013, https://doi.org/10.1111/mmi.12237
  3. Interaction Between the Quorum Sensing and Stringent Response Regulation Systems in the Enterohemorrhagic Escherichia coli O157:H7 EDL933 Strain vol.24, pp.3, 2010, https://doi.org/10.4014/jmb.1310.10091
  4. Quorum-sensing gene luxS regulates flagella expression and Shiga-like toxin production in F18ab Escherichia coli vol.60, pp.6, 2010, https://doi.org/10.1139/cjm-2014-0178