1887

Abstract

The chromosome contains a seven-gene polycistronic unit (the operon) whose products share extensive homologies with their counterparts in serovar Typhimurium (), another Gram-negative bacterial enteropathogen. This gene cluster is essential for addition of 4-aminoarabinose to the lipid moiety of LPS, as demonstrated by MALDI-TOF mass spectrometry of lipid A from both wild-type and -mutated strains. As in , 4-aminoarabinose substitution of lipid A contributes to resistance of to the antimicrobial peptide polymyxin B. Whereas expression in is mediated by both the PhoP–PhoQ and PmrA–PmrB two-component regulatory systems, it appears to be PmrA–PmrB-independent in , with the response regulator PhoP interacting directly with the operon promoter region. This result reveals that the ubiquitous PmrA–PmrB regulatory system controls different regulons in distinct bacterial species. In addition, inactivation in has no effect on bacterial virulence in the mouse, again in contrast to the situation in . The marked differences in operon regulation in these two phylogenetically close bacterial species may be related to their dissimilar lifestyles.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27426-0
2004-12-01
2019-11-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/12/mic1503947.html?itemId=/content/journal/micro/10.1099/mic.0.27426-0&mimeType=html&fmt=ahah

References

  1. Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A. & Carniel, E. ( 1999; ). Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 96, 14043–14048.[CrossRef]
    [Google Scholar]
  2. Aussel, L., Therisod, H., Karibian, D., Perry, M. B., Bruneteau, M. & Caroff, M. ( 2000; ). Novel variation of lipid A structures in strains of different Yersinia species. FEBS Lett 465, 87–92.[CrossRef]
    [Google Scholar]
  3. Bellefontaine, A. F., Pierreux, C. E., Mertens, P., Vandenhaute, J., Letesson, J. J. & De Bolle, X. ( 2002; ). Plasticity of a transcriptional regulation network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus. Mol Microbiol 43, 945–960.[CrossRef]
    [Google Scholar]
  4. Bengoechea, J. A., Lindner, B., Seydel, U., Diaz, R. & Moriyon, I. ( 1998a; ). Yersinia pseudotuberculosis and Yersinia pestis are more resistant to bactericidal cationic peptides than Yersinia enterocolitica. Microbiology 144, 1509–1515.[CrossRef]
    [Google Scholar]
  5. Bengoechea, J. A., Brandenburg, K., Seydel, U., Diaz, R. & Moriyon, I. ( 1998b; ). Yersinia pseudotuberculosis and Yersinia pestis show increased outer membrane permeability to hydrophobic agents which correlates with lipopolysaccharide acyl-chain fluidity. Microbiology 144, 1517–1526.[CrossRef]
    [Google Scholar]
  6. Bhagya Lakshmi, S. K., Bhat, U. R., Wartenberg, K., Schlecht, S. & Mayer, H. ( 1989; ). Temperature-dependent incorporation of 4-amino-l-arabinose in lipid A of distinct gram-negative bacteria. FEMS Microbiol Lett 51, 317–322.
    [Google Scholar]
  7. Caillet, J. & Droogmans, L. ( 1988; ). Molecular cloning of the Escherichia coli miaA gene involved in the formation of delta 2-isopentenyl adenosine in tRNA. J Bacteriol 170, 4147–4152.
    [Google Scholar]
  8. Carnoy, C., Mullet, C., Muller-Alouf, H., Leteurtre, E. & Simonet, M. ( 2000; ). Superantigen YPMa exacerbates the virulence of Yersinia pseudotuberculosis in mice. Infect Immun 68, 2553–2559.[CrossRef]
    [Google Scholar]
  9. Chain, P. S. G., Carniel, E., Larimer, F. W. & 20 other authors ( 2004; ). Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 101, 13826–13831.[CrossRef]
    [Google Scholar]
  10. Conchas, R. F. & Carniel, E. ( 1990; ). A highly efficient electroporation system for transformation of Yersinia. Gene 87, 133–137.[CrossRef]
    [Google Scholar]
  11. Cornelis, G. R. ( 2002; ). The Yersinia Ysc-Yop ‘type III’ weaponry. Nat Rev Mol Cell Biol 3, 742–752.[CrossRef]
    [Google Scholar]
  12. Derzelle, S., Turlin, E., Duchaud, E., Pages, S., Kunst, F., Givaudan, A. & Danchin, A. ( 2004; ). The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 186, 1270–1279.[CrossRef]
    [Google Scholar]
  13. de Veaux, L. C., Clevenson, D. S., Bradbeer, C. & Kadner, R. J. ( 1986; ). Identification of the btuCED polypeptides and evidence for their role in vitamin B12 transport in Escherichia coli. J Bacteriol 167, 920–927.
    [Google Scholar]
  14. Devine, D. A. & Hancock, R. E. ( 2002; ). Cationic peptides: distribution and mechanisms of resistance. Curr Pharm Des 8, 703–714.[CrossRef]
    [Google Scholar]
  15. Donnenberg, M. S. & Kaper, J. B. ( 1991; ). Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59, 4310–4317.
    [Google Scholar]
  16. Durand, J. M., Björk, G. R., Kuwae, A., Yoshikawa, M. & Sasakawa, C. ( 1997; ). The modified nucleoside 2-methylthio-N 6-isopentenyladenosine in tRNA of Shigella flexneri is required for expression of virulence genes. J Bacteriol 179, 5777–5782.
    [Google Scholar]
  17. Durand, J. M., Dagberg, B., Uhlin, B. E. & Björk, G. R. ( 2000; ). Transfer RNA modification, temperature and DNA superhelicity have a common target in the regulatory network of the virulence of Shigella flexneri: the expression of the virF gene. Mol Microbiol 35, 924–935.[CrossRef]
    [Google Scholar]
  18. Garcia Vescovi, E., Soncini, F. C. & Groisman, E. A. ( 1996; ). Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84, 165–174.[CrossRef]
    [Google Scholar]
  19. Gottesman, S., Halpern, E. & Trisler, P. ( 1981; ). Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J Bacteriol 148, 265–273.
    [Google Scholar]
  20. Gray, J., Wang, J. & Gelvin, S. B. ( 1992; ). Mutation of the miaA gene of Agrobacterium tumefaciens results in reduced vir gene expression. J Bacteriol 174, 1086–1098.
    [Google Scholar]
  21. Groisman, E. A., Kayser, J. & Soncini, F. C. ( 1997; ). Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J Bacteriol 179, 7040–7045.
    [Google Scholar]
  22. Gunn, J. S., Lim, K. B., Krueger, J., Kim, K., Guo, L., Hackett, M. & Miller, S. I. ( 1998; ). PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27, 1171–1182.[CrossRef]
    [Google Scholar]
  23. Gunn, J. S., Ryan, S. S., Van Velkinburgh, J. C., Ernst, R. K. & Miller, S. I. ( 2000; ). Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar typhimurium. Infect Immun 68, 6139–6146.[CrossRef]
    [Google Scholar]
  24. Hancock, R. E. & Rozek, A. ( 2002; ). Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol Lett 206, 143–149.[CrossRef]
    [Google Scholar]
  25. Hancock, R. E. & Scott, M. G. ( 2000; ). The role of antimicrobial peptides in animal defenses. Proc Natl Acad Sci U S A 97, 8856–8861.[CrossRef]
    [Google Scholar]
  26. Himpens, S., Locht, C. & Supply, P. ( 2000; ). Molecular characterization of the mycobacterial SenX3-RegX3 two-component system: evidence for autoregulation. Microbiology 146, 3091–3098.
    [Google Scholar]
  27. Hyytiäinen, H., Sjöblom, S., Palomäki, T., Tuikkala, A. & Tapio Palva, E. ( 2003; ). The PmrA-PmrB two-component system responding to acidic pH and iron controls virulence in the plant pathogen Erwinia carotovora ssp. carotovora. Mol Microbiol 50, 795–807.[CrossRef]
    [Google Scholar]
  28. Kawahara, K., Tsukano, H., Watanabe, H., Lindner, B. & Matsuura, M. ( 2002; ). Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect Immun 70, 4092–4098.[CrossRef]
    [Google Scholar]
  29. Korat, B., Mottl, H. & Keck, W. ( 1991; ). Penicillin-binding protein 4 of Escherichia coli: molecular cloning of the dacB gene, controlled overexpression, and alterations in murein composition. Mol Microbiol 5, 675–684.[CrossRef]
    [Google Scholar]
  30. Kox, L. F., Wosten, M. M. & Groisman, E. A. ( 2000; ). A small protein that mediates the activation of a two-component system by another two-component system. EMBO J 19, 1861–1872.[CrossRef]
    [Google Scholar]
  31. Lee, H., Hsu, F. F., Turk, J. & Groisman, E. A. ( 2004; ). The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J Bacteriol 186, 4124–4133.[CrossRef]
    [Google Scholar]
  32. Lindner, B. ( 2000; ). Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry of lipopolysaccharides. Methods Mol Biol 145, 311–325.
    [Google Scholar]
  33. Marceau, M., Dubuquoy, L., Caucheteux-Rousseaux, C., Foligne, B., Desreumaux, P. & Simonet, M. ( 2004; ). Yersinia pseudotuberculosis anti-inflammatory components reduce trinitrobenzene sulfonic acid-induced colitis in the mouse. Infect Immun 72, 2438–2441.[CrossRef]
    [Google Scholar]
  34. McPhee, J. B., Lewenza, S. & Hancock, R. E. ( 2003; ). Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50, 205–217.[CrossRef]
    [Google Scholar]
  35. Miller, V. L. & Mekalanos, J. J. ( 1988; ). A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170, 2575–2583.
    [Google Scholar]
  36. Moskowitz, S. M., Ernst, R. K. & Miller, S. I. ( 2004; ). PmrAB, a two-component regulatory system of Pseudomonas aeruginosa that modulates resistance to cationic antimicrobial peptides and addition of aminoarabinose to lipid A. J Bacteriol 186, 575–579.[CrossRef]
    [Google Scholar]
  37. Oyston, P. C., Dorrell, N., Williams, K., Li, S. R., Green, M., Titball, R. W. & Wren, B. W. ( 2000; ). The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 68, 3419–3425.[CrossRef]
    [Google Scholar]
  38. Parkhill, J., Wren, B. W., Thomson, N. R. & 32 other authors ( 2001; ). Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523–527.[CrossRef]
    [Google Scholar]
  39. Rebeil, R., Ernst, R. K., Gowen, B. B., Miller, S. I. & Hinnebusch, B. J. ( 2004; ). Variation in lipid A structure in the pathogenic yersiniae. Mol Microbiol 52, 1363–1373.[CrossRef]
    [Google Scholar]
  40. Reed, L. J. & Muench, H. A. ( 1938; ). A simple method of estimating fifty per cent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  41. Riot, B., Berche, P. & Simonet, M. ( 1997; ). Urease is not involved in the virulence of Yersinia pseudotuberculosis in mice. Infect Immun 65, 1985–1990.
    [Google Scholar]
  42. Roland, K. L., Esther, C. R. & Spitznagel, J. K. ( 1994; ). Isolation and characterization of a gene, pmrD, from Salmonella typhimurium that confers resistance to polymyxin when expressed in multiple copies. J Bacteriol 176, 3589–3597.
    [Google Scholar]
  43. Sambrook, J. & Russell, D. W. ( 2001; ). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  44. Sebbane, F., Devalckenaere, A., Foulon, J., Carniel, E. & Simonet, M. ( 2001; ). Silencing and reactivation of urease in Yersinia pestis is determined by one G residue at a specific position in the ureD gene. Infect Immun 69, 170–176.[CrossRef]
    [Google Scholar]
  45. Simon, R., Priefer, U. & Puhler, A. ( 1983; ). A broad host range mobilization system for in vitro genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio Technology 1, 784–791.[CrossRef]
    [Google Scholar]
  46. Soncini, F. C., Garcia Vescovi, E., Solomon, F. & Groisman, E. A. ( 1996; ). Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 178, 5092–5099.
    [Google Scholar]
  47. Wosten, M. M. & Groisman, E. A. ( 1999; ). Molecular characterization of the PmrA regulon. J Biol Chem 274, 27185–27190.[CrossRef]
    [Google Scholar]
  48. Wosten, M. M., Kox, L. F., Chamnongpol, S., Soncini, F. C. & Groisman, E. A. ( 2000; ). A signal transduction system that responds to extracellular iron. Cell 103, 113–125.[CrossRef]
    [Google Scholar]
  49. Wu, M., Maier, E., Benz, R. & Hancock, R. E. ( 1999; ). Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38, 7235–7242.[CrossRef]
    [Google Scholar]
  50. Zhou, Z., Lin, S., Cotter, R. J. & Raetz, C. R. ( 1999; ). Lipid A modifications characteristic of Salmonella typhimurium are induced by NH4VO3 in Escherichia coli K12. Detection of 4-amino-4-deoxy-l-arabinose, phosphoethanolamine and palmitate. J Biol Chem 274, 18503–18514.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27426-0
Loading
/content/journal/micro/10.1099/mic.0.27426-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error