1887

Abstract

biofilm formation causes massive adsorption of haemin or Congo red as well as colonization and eventual blockage of the flea proventriculus . This blockage allows effective transmission of plague from some fleas, like the oriental rat flea, to mammals. Four Hms proteins, HmsH, HmsF, HmsR and HmsS, are essential for biofilm formation, with HmsT and HmsP acting as positive and negative regulators, respectively. HmsH has a -barrel structure with a large periplasmic domain while HmsF possesses polysaccharide deacetylase and COG1649 domains. HmsR is a putative glycosyltransferase while HmsS has no recognized domains. In this study, specific amino acids within conserved domains or within regions of high similarity in HmsH, HmsF, HmsR and HmsS proteins were selected for site-directed mutagenesis. Some but not all of the substitutions in HmsS and within the periplasmic domain of HmsH were critical for protein function. Substitutions within the glycosyltransferase domain of HmsR and the deacetylase domain of HmsF abolished biofilm formation in . Surprisingly, substitution of highly conserved residues within COG1649 did not affect HmsF function.

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2006-11-01
2020-07-03
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References

  1. Ausubel F. M, Brent R, Kingston R. E, Moore D. D, Seidman J. G, Smith J. A, Struhl K. 1987; Current Protocols in Molecular Biology New York: Wiley;
    [Google Scholar]
  2. Bacot A. W. 1915; LXXXI. Further notes on the mechanism of the transmission of plague by fleas. J Hyg14:774–776
    [Google Scholar]
  3. Bacot A. W, Martin C. J. 1914; LXVII. Observations on the mechanism of the transmission of plague by fleas. J Hyg13:423–439
    [Google Scholar]
  4. Bagos P. G, Liakopoulos T. D, Spyropoulos I. C, Hamodrakas S. J. 2004; PRED-TMBB: a web server for predicting the topology of β -barrel outer membrane proteins. Nucleic Acids Res32:W400–W404[CrossRef]
    [Google Scholar]
  5. Bao Q, Tian Y, Li W.18 other authors 2002; A complete sequence of the T. tengcongensis genome. Genome Res12:689–700[CrossRef]
    [Google Scholar]
  6. Bateman A, Coin L, Durbin R.10 other authors 2004; The Pfam protein families database. Nucleic Acids Res32:D138–D141[CrossRef]
    [Google Scholar]
  7. Bearden S. W, Perry R. D. 1999; The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol32:403–414[CrossRef]
    [Google Scholar]
  8. Bell K. S, Sebaihia M, Pritchard L. 29 other authors 2004; Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A101:11105–11110[CrossRef]
    [Google Scholar]
  9. Birnboim H. C, Doly J. 1979; A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res7:1513–1523[CrossRef]
    [Google Scholar]
  10. Blair D. E, van Aalten D. M. F. 2004; Structures of Bacillus subtilis PdaA, a family 4 carbohydrate esterase, and a complex with N -acetylglucosamine. FEBS Lett570:13–19[CrossRef]
    [Google Scholar]
  11. Blattner F. R, Bloch C. A, Plunkett G. III. 14 other authors 1997; The complete genome sequence of Escherichia coli K-12. Science277:1453–1474[CrossRef]
    [Google Scholar]
  12. Bobrov A. G, Kirillina O, Perry R. D. 2005; The phosphodiesterase activity of the HmsP EAL domain is required for negative regulation of biofilm formation in Yersinia pestis . FEMS Microbiol Lett247:123–130[CrossRef]
    [Google Scholar]
  13. Branda S. S, Friedman L, Kolter R, Vik . 2005; Biofilms: the matrix revisited. Trends Microbiol13:20–26[CrossRef]
    [Google Scholar]
  14. Darby C, Hsu J. W, Ghori N, Falkow S. 2002; Caenorhabditis elegans : plague bacteria biofilm blocks food intake. Nature417:243–244[CrossRef]
    [Google Scholar]
  15. Darby C, Ananth S. L, Tan L, Hinnebusch B. J. 2005; Identification of gmhA , a Yersinia pestis gene required for flea blockage, by using a Caenorhabditis elegans biofilm system. Infect Immun73:7236–7242[CrossRef]
    [Google Scholar]
  16. da Silva A. C. R, Ferro J. A, Reinach F. C.62 other authors 2002; Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature417:459–463[CrossRef]
    [Google Scholar]
  17. Datsenko K. A, Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A97:6640–6645[CrossRef]
    [Google Scholar]
  18. Davey M. E, O'Toole G. A. 2000; Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev64:847–867[CrossRef]
    [Google Scholar]
  19. Deng W, Burland V, Plunkett G. III. 18 other authors 2002; Genome sequence of Yersinia pestis KIM. J Bacteriol184:4601–4611[CrossRef]
    [Google Scholar]
  20. Fetherston J. D, Schuetze P, Perry R. D. 1992; Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol Microbiol6:2693–2704[CrossRef]
    [Google Scholar]
  21. Fetherston J. D, Perry R. D, Lillard J. W. Jr. 1995; Analysis of the pesticin receptor from Yersinia pestis : role in iron-deficient growth and possible regulation by its siderophore. J Bacteriol177:1824–1833
    [Google Scholar]
  22. Fukushima T, Yamamoto H, Atrih A, Foster S. J, Sekiguchi J. 2002; A polysaccharide deacetylase gene (pdaA) is required for germination and for production of muramic δ -lactam residues in the spore cortex of Bacillus subtilis . J Bacteriol184:6007–6015[CrossRef]
    [Google Scholar]
  23. Fukushima T, Tanabe T, Yamamoto H, Hosoya S, Sato T, Yoshikawa H, Sekiguchi J. 2004; Characterization of a polysaccharide deacetylase gene homologue (pdaB) on sporulation of Bacillus subtilis . J Biochem136:283–291[CrossRef]
    [Google Scholar]
  24. Fukushima T, Kitajima T, Sekiguchi J. 2005; A polysaccharide deacetylase homologue, PdaA, in Bacillus subtilis acts as an N -acetylmuramic acid deacetylase in vitro. J Bacteriol187:1287–1292[CrossRef]
    [Google Scholar]
  25. Gilmore M. E, Bandyopadhyay D, Dean A. M, Linnstaedt S. D, Popham D. L. 2004; Production of muramic δ -lactam in Bacillus subtilis spore peptidoglycan. J Bacteriol186:80–89[CrossRef]
    [Google Scholar]
  26. Guzman L. M, Belin D, Carson M. J, Beckwith J. 1995; Tight regulation, modulation, and high-level expression by vectors containing the arabinose P[sub]BAD[/sub] promoter. J Bacteriol177:4121–4130
    [Google Scholar]
  27. Hare J. M, McDonough K. A. 1999; High-frequency RecA-dependent and -independent mechanisms of Congo red binding mutations in Yersinia pestis . J Bacteriol181:4896–4904
    [Google Scholar]
  28. Hartzell P. L, Millstein J, LaPaglia C. 1999; Biofilm formation in hyperthermophilic Archaea. Methods Enzymol310:335–349
    [Google Scholar]
  29. Heilmann C, Schweitzer O, Gerke C, Vanittannakom N, Mack D, Götz F. 1996; Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis . Mol Microbiol20:1083–1091[CrossRef]
    [Google Scholar]
  30. Hinnebusch B. J, Perry R. D, Schwan T. G. 1996; Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science273:367–370[CrossRef]
    [Google Scholar]
  31. Humphreys G. O, Willshaw G. A, Anderson E. S. 1975; A simple method for the preparation of large quantities of pure plasmid DNA. Biochim Biophys Acta383:457–463[CrossRef]
    [Google Scholar]
  32. Itoh Y, Wang X, Hinnebusch B. J, Romeo T, Preston J. F. III. 2005; Depolymerization of β -1,6- N -acetyl-d-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol187:382–387[CrossRef]
    [Google Scholar]
  33. Jarrett C. O, Deak E, Isherwood K. E, Oyston P. C, Fischer E. R, Whitney A. R, Kobayashi S. D, DeLeo F. R, Hinnebusch B. J. 2004; Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J Infect Dis190:783–792[CrossRef]
    [Google Scholar]
  34. Jones H. A, Perry R. D, Lillard J. W. Jr. 1999; HmsT, a protein essential for expression of the haemin storage (Hms[sup]+[/sup]) phenotype of Yersinia pestis . Microbiology145:2117–2128[CrossRef]
    [Google Scholar]
  35. Kaniga K, Delor I, Cornelis G. R. 1991; A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica . Gene109:137–141[CrossRef]
    [Google Scholar]
  36. Kaplan J. B, Meyenhofer M. F, Fine D. H. 2003; Biofilm growth and detachment of Actinobacillus actinomycetemcomitans . J Bacteriol185:1399–1404[CrossRef]
    [Google Scholar]
  37. Kirillina O, Fetherston J. D, Bobrov A. G, Abney J, Perry R. D. 2004; HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis . Mol Microbiol54:75–88[CrossRef]
    [Google Scholar]
  38. Lee B.-M, Park Y.-J, Park D.-S.16 other authors 2005; The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res33:577–586[CrossRef]
    [Google Scholar]
  39. Lillard J. W. Jr, Fetherston J. D, Pedersen L, Pendrak M. L, Perry R. D. 1997; Sequence and genetic analysis of the hemin storage (hms) system of Yersinia pestis . Gene193:13–21[CrossRef]
    [Google Scholar]
  40. Lillard J. W. Jr, Bearden S. W, Fetherston J. D, Perry R. D. 1999; The haemin storage (Hms[sup]+[/sup]) phenotype of Yersinia pestis is not essential for the pathogenesis of bubonic plague in mammals. Microbiology145:197–209[CrossRef]
    [Google Scholar]
  41. Methé B. A, Nelson K. E, Eisen J. A.31 other authors 2003; Genome of Geobacter sulfurreducens : metal reduction in subsurface environments. Science302:1967–1969[CrossRef]
    [Google Scholar]
  42. Nascimento A. L. T. O, Ko A. I, Martins E. A. L. 44 other authors 2004; Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J Bacteriol186:2164–2172[CrossRef]
    [Google Scholar]
  43. Notredame C, Higgins D. G, Heringa J. 2000; T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol302:205[CrossRef]
    [Google Scholar]
  44. O'Toole G. A, Pratt L. A, Watnick P. I, Newman D. K, Weaver V. B, Kolter R. 1999; Genetic approaches to study of biofilms. Methods Enzymol310:91–109
    [Google Scholar]
  45. Paulsen I. T, Press C. M, Ravel J.26 other authors 2005; Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol23:873–878[CrossRef]
    [Google Scholar]
  46. Pendrak M. L, Perry R. D. 1991; Characterization of a hemin-storage locus of Yersinia pestis . Biol Metals4:41–47[CrossRef]
    [Google Scholar]
  47. Pendrak M. L, Perry R. D. 1993; Proteins essential for expression of the Hms[sup]+[/sup] phenotype of Yersinia pestis . Mol Microbiol8:857–864[CrossRef]
    [Google Scholar]
  48. Perry R. D, Fetherston J. D. 1997; Yersinia pestis - etiologic agent of plague. Clin Microbiol Rev10:35–66
    [Google Scholar]
  49. Perry R. D, Pendrak M. L, Schuetze P. 1990; Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis . J Bacteriol172:5929–5937
    [Google Scholar]
  50. Perry R. D, Lucier T. S, Sikkema D. J, Brubaker R. R. 1993; Storage reservoirs of hemin and inorganic iron in Yersinia pestis . Infect Immun61:32–39
    [Google Scholar]
  51. Perry R. D, Bobrov A. G, Kirillina O, Jones H. A, Pedersen L. L, Abney J, Fetherston J. D. 2004; Temperature regulation of the hemin storage (Hms[sup]+[/sup]) phenotype of Yersinia pestis is posttranscriptional. J Bacteriol186:1638–1647[CrossRef]
    [Google Scholar]
  52. Pollitzer R. 1954; Plague. World Health Organ Monogr Ser22:1–698
    [Google Scholar]
  53. Ren S.-X, Fu G, Jiang X.-G.36 other authors 2003; Unique physiological and pathogenic features of Leptospira interrogans revealed by whole-genome sequencing. Nature422:888–893[CrossRef]
    [Google Scholar]
  54. Salanoubat M, Genin S, Artiguenave F.25 other authors 2002; Genome sequence of the plant pathogen Ralstonia solanacearum . Nature415:497–502[CrossRef]
    [Google Scholar]
  55. Sambrook J, Russell D. W. 2001; Molecular Cloning: a Laboratory Manual, 3rd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  56. Saxena I. M, Brown R. M. Jr. 1997; Identification of cellulose synthase(s) in higher plants: sequence analysis of processive β -glycosyltransferases with the common motif “D,D, D35Q(R,Q)XRW”. Cellulose 4:33–49[CrossRef]
    [Google Scholar]
  57. Saxena I. M, Brown J, Malcolm R, Dandekar T. 2001; Structure-function characterization of cellulose synthase: relationship to other glycosyltransferases. Phytochemistry57:1135–1148[CrossRef]
    [Google Scholar]
  58. Simm R, Fetherston J. D, Kader A, Perry R. D, Römling U. 2005; Phenotypic convergence mediated by GGDEF-domain-containing proteins. J Bacteriol187:6816–6823[CrossRef]
    [Google Scholar]
  59. Spiers A. J, Kahn S. G, Bohannon J, Travisano M, Rainey P. B. 2002; Adaptive divergence in experimental populations of Pseudomonas fluorescens . I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics161:33–46
    [Google Scholar]
  60. Straley S. C, Bowmer W. S. 1986; Virulence genes regulated at the transcriptional level by Ca[sup]2+[/sup] in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun51:445–454
    [Google Scholar]
  61. Tan L, Darby C. 2004; A movable surface: formation of Yersinia sp. biofilms on motile Caenorhabditis elegans . J Bacteriol186:5087–5092[CrossRef]
    [Google Scholar]
  62. Towbin H, Staehelin T, Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A76:4350–4354[CrossRef]
    [Google Scholar]
  63. Wang R. F, Kushner S. R. 1991; Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli . Gene100:195–199[CrossRef]
    [Google Scholar]
  64. Wang X, Romeo T, Preston J. F. III. 2004; The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol186:2724–2734[CrossRef]
    [Google Scholar]
  65. Wood P. J. 1980; Specificity in the interaction of direct dyes with polysaccharides. Carbohydr Res85:271–287[CrossRef]
    [Google Scholar]
  66. Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. 2001; The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol39:1452–1463[CrossRef]
    [Google Scholar]
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