Initial Characterization of yliH in Salmonella typhimurium

  • Park, Kyung-Hwa (Genome Research Center for Enteropathogenic Bacteria and Research Institute of Vibrio infection, Chonnam National University Medical School) ;
  • Song, Mi-Ryung (Genome Research Center for Enteropathogenic Bacteria and Research Institute of Vibrio infection, Chonnam National University Medical School) ;
  • Choy, Hyon-E. (Genome Research Center for Enteropathogenic Bacteria and Research Institute of Vibrio infection, Chonnam National University Medical School)
  • Published : 2007.12.31

Abstract

Using microarray analysis, we determined those Salmonella genes induced at the entry of stationary phase, and subsequently discovered that uncharacterized yliH was induced most dramatically. We set out to establish the molecular mechanism underlying the stationary phase induction of yliH under the standard culture condition, LB with vigorous aeration, by analyzing its promoter activity in various mutant backgrounds, lacking stationary phase ${\sigma}$, $RpoS^-$, or stringent signal molecules ppGpp, ${\Delta}relA$ ${\Delta}spoT$. It was found that the stationary phase induction of yliHp was partially dependent on rpoS but entirely dependent on ppGpp. DNA sequence analysis revealed that the Salmonella yliH gene is composed of 381 base-pair nucleotides, with overall amino acid sequence revealing 76.38% amino acid identity and 88.98% similarity with Escherichia coli yliH, although no motif from data base was noted for its possible role. Recently however, it has been reported that yliH in E. coli was implicated in biofilm formation and motility by repressing these activities (Domka et al., 2006). We have constructed a mutant Salmonella deleting yliH gene by allele replacement and examined its phenotype, and found that the yliH in Salmonella more or less affects motility and adherence by enhancing these activities. The effect on biofilm formation in Salmonella was uncertain. Moreover, addition of cloned yliH of E. coli into Salmonella did not reduce motility or adherence. Taken together, it appears that the pathways implicating yliH for biofilm formation and motility in E. coli and in Salmonella are somewhat different.

Keywords

References

  1. Alam, M., S.-I. Miyoshi, S. Yamamoto, K.-I. Tomochika, and S. Shinoda. 1996. Expression of virulence-related properties by, and intestinal adhesiveness of, Vibrio mimicus strains isolated from aquatic environments. Appl. Environ. Microbiol. 62, 3871-3874
  2. Barker, M.M., T. Gaal, and R.L. Gourse. 2001. Mechanism of regulation of transcription initiation by ppGpp. II. Models for positive control based on properties of RNAP mutants and competition for RNAP. J. Mol. Biol. 305, 689-702 https://doi.org/10.1006/jmbi.2000.4328
  3. Cashel, M., D.R. Gentry, V.J. Hernandez, and D. Vinella. 1996. Escherichia coli and Salmonella, p. 1458-1496. In F.C. Neidhardt, R. Curtiss III, J.L. Ingraham, E.C.C. Lin, K.B. Low, B. Magasanik, W.S. Reznikoff, M. Riley, M. Schaechter, and H.E. Umbarger (eds.), Cellular and molecular biology. American Society for Microbiology, Washington, D.C., USA
  4. Choy, H.E. 2000. The study of guanosine 5'-diphosphate 3'-diphosphate- mediated transcription regulation in vitro using a coupled transcription-translation system. J. Biol. Chem. 275, 6783-6789 https://doi.org/10.1074/jbc.275.10.6783
  5. Christensen, G.D., W.A. Simpson, A.L. Bisno, and E.H. Beachey. 1982. Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect. Immun. 37, 318-326
  6. Coburn, B., Y. Li, D. Owen, B.A. Vallance, and B.B. Finlay. 2005. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect. Immun. 73, 3219-3227 https://doi.org/10.1128/IAI.73.6.3219-3227.2005
  7. 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. USA 97, 6640-6645
  8. Davis, R.W., D. Botstein, and J.R. Roth. 1980. Advanced bacterial genetics. In A manual for genetic engineering. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA
  9. Domka, J., J. Lee, and T.K. Wood. 2006. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl. Environ. Microbiol. 72, 2449-2459 https://doi.org/10.1128/AEM.72.4.2449-2459.2006
  10. Fierer, J. and M. Swancutt. 2000. Non-typhoid Salmonella: a review. Curr. Clin. Top. Infect. Dis. 20, 134-157
  11. Fux, C.A., J.W. Costerton, P.S. Stewart, and P. Stoodley. 2005. Survival strategies of infectious biofilms. Trends Microbiol. 13, 34-40 https://doi.org/10.1016/j.tim.2004.11.010
  12. Gentry, D.R., V.J. Hernandez, L.H. Nguyen, D.B. Jensen, and M. Cashel. 1993. Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp. J. Bacteriol. 175, 7982-7989 https://doi.org/10.1128/jb.175.24.7982-7989.1993
  13. Hengge-Aronis, R. 2002. Recent insights into the general stress response regulatory network in Escherichia coli. J. Mol. Microbiol. Biotechnol. 4, 341-346
  14. Jishage, M., K. Kvint, V. Shingler, and T. Nystrom. 2002. Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev. 16, 1260-1270 https://doi.org/10.1101/gad.227902
  15. Kano, Y., A. Matsushiro, and Y. Shimura. 1968. Isolation of the novel regulatory mutants of the tryptophan biosynthetic system in Escherichia coli. Mol. Gen. Genet. 102, 15-26
  16. Kvint, K., A. Farewell, and T. Nystrom. 2000. RpoS-dependent promoters require guanosine tetraphosphate for induction even in the presence of high levels of sigma(s). J. Biol. Chem. 275, 14795-14798 https://doi.org/10.1074/jbc.C000128200
  17. Loewen, P.C. and R. Hengge-Aronis. 1994. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu. Rev. Microbiol. 48, 53-80 https://doi.org/10.1146/annurev.mi.48.100194.000413
  18. Magnusson, L.U., B. Gummersson, P. Joksimovic, A. Farewlla, and T. Nystrom. 2007. Identical, independent, and opposing roles of ppGpp and DksA in Escherichia coli. J. Bacteriol. 189, 5193-5202 https://doi.org/10.1128/JB.00330-07
  19. Marshall, K.C. 1992. Biofilms: an overview of bacterial adhesion, activity, and control at surfaces. ASM News 58, 202-207
  20. Marshall, K.C., R. Stout, and R. Mitchell. 1971. Mechanisms of the initial events in the sorption of marine bacteria to surfaces. J. Gen. Microbiol. 68, 337-348 https://doi.org/10.1099/00221287-68-3-337
  21. McClelland, M., K.E. Sanderson, J. Spieth, S.W. Clifton, P. Latreille, L. Courtney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R.K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413, 852-856 https://doi.org/10.1038/35101614
  22. Miller, J.H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA
  23. O'Toole, G.A., L.A. Pratt, P.I. Watnick, D.K. Newman, V.B. Weaver, and R. Kolter. 1999. Genetic approaches to study of biofilms. Methods Enzymol. 310, 91-109 https://doi.org/10.1016/S0076-6879(99)10008-9
  24. Paul, B.J., M.B. Berkmen, and R.L. Gourse. 2005. DksA potentiates direct activation of amino acid promoters by ppGpp. Proc. Natl. Acad. Sci. USA 102, 7823-7828
  25. Popoff, M.Y. and L.L. Minor. 1997. Antigenic formulae of the Salmonella serovars. WHO Collaborating Center for Reference and Research, Institue Pasteur, Paris, France
  26. Pratt, L.A. and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30, 285-293 https://doi.org/10.1046/j.1365-2958.1998.01061.x
  27. Prouty, A.M., W.H. Schwesinger, and J.S. Gunn. 2002. Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp.. Infect. Immun. 70, 2640-2649 https://doi.org/10.1128/IAI.70.5.2640-2649.2002
  28. Putnam, S.L. and A.L. Koch. 1975. Complications in the simplest cellular enzyme assay: lysis of Escherichia coli for the assay of beta-galactosidase. Anal. Biochem. 63, 350-360 https://doi.org/10.1016/0003-2697(75)90357-7
  29. Ren, D., L.A. Bedzyk, S.M. Thomas, R.W. Ye, and T.K. Wood. 2004. Gene expression in Escherichia coli biofilms. Appl. Microbiol. Biotechnol. 64, 515-524 https://doi.org/10.1007/s00253-003-1517-y
  30. Romling, U., W.D. Sierralta, K. Eriksson, and S. Normark. 1998. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28, 249-264 https://doi.org/10.1046/j.1365-2958.1998.00791.x
  31. Simons, R.W., F. Houman, and N. Kleckner. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53, 85-96 https://doi.org/10.1016/0378-1119(87)90095-3
  32. Song, M., H.J. Kim, E.Y. Kim, M. Shin, H.C. Lee, Y. Hong, J.H. Rhee, H. Yoon, S. Ryu, S. Lim, and H.E. Choy. 2004. ppGppdependent stationary phase induction of genes on Salmonella pathogenicity island 1. J. Biol. Chem. 279, 34183-34190 https://doi.org/10.1074/jbc.M313491200
  33. Torres, A.G., X. Zhou, and J.B. Kaper. 2005. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect. Immun. 73, 18-29 https://doi.org/10.1128/IAI.73.1.18-29.2005
  34. Watnick, P. and R. Kolter. 2000. Biofilm, city of microbes. J. Bacteriol. 182, 2675-2679 https://doi.org/10.1128/JB.182.10.2675-2679.2000
  35. Whitfield, C. and W.J. Keenleyside. 1995. Regulation of expression of group IA capsular polysaccharides in Escherichia coli and related extracellular polysaccharides in other bacteria. J. Ind. Microbiol. 15, 361-371 https://doi.org/10.1007/BF01569992
  36. Xiao, H., M. Kalman, K. Ikehara, S. Zemel, G. Glaser, and M. Cashel. 1991. Residual guanosine 3',5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J. Biol. Chem. 266, 5980-50901995
  37. Zhou, Y.N. and D.J. Jin. 1998. The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like 'stringent' RNA polymerases in Escherichia coli. Proc. Natl. Acad. Sci. USA 95, 2908-2913