1887

Abstract

Osmoregulated periplasmic glucans (OPGs) are produced by many proteobacteria and are important for bacterial–host interactions. The and genes involved in the synthesis of OPGs are the most widely distributed genes in proteobacterial genomes. Two other non-homologous genes, both named , are also involved in OPG biosynthesis in several species. The genome possesses two ORFs, PA5077 and PA5078, that show similarity to and of , respectively, and one ORF, PA1163, similar to of . Here, we report that the locus of PA14 is involved in the synthesis of linear polymers with -1,2-linked glucosyl residues branched with a few -1,6 glucosyl residues. Succinyl residues also substitute this glucose backbone. Transcription of is repressed by high osmolarity. Low osmolarity promotes the formation of highly structured biofilms, but biofilm development is slower and the area of biomass is reduced under high osmolarity. Biofilm development of an mutant grown under low osmolarity presents a similar phenotype to the wild-type biofilm grown under high osmolarity. These results suggest that OPGs are important for biofilm formation under conditions of low osmolarity. A previous study suggested that the gene is involved in the resistance of biofilms to antibiotics. We have shown that is not involved in the biosynthesis of the OPG described here, and do not appear to be involved in the resistance of PA14 biofilms to antibiotics.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/008953-0
2007-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/10/3255.html?itemId=/content/journal/micro/10.1099/mic.0.2007/008953-0&mimeType=html&fmt=ahah

References

  1. Bohin J. P., Lacroix J. M. 2006; Osmoregulation in the periplasm. In The Periplasm 325–341 Edited by Ehrmann M. Washington, DC: ASM Press;
    [Google Scholar]
  2. Bradley D. E. 1980; A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can J Microbiol 26:146–154
    [Google Scholar]
  3. Breedveld M. W., Miller K. J. 1994; Cyclic β -glucans of members of the family Rhizobiaceae . Microbiol Rev 58:145–161
    [Google Scholar]
  4. Burns J. L., Ramsey B. W., Smith A. L. 1993; Clinical manifestations and treatment of pulmonary infections in cystic fibrosis. Adv Pediatr Infect Dis 8:53–66
    [Google Scholar]
  5. Costerton J. W. 1995; Overview of microbial biofilms. J Ind Microbiol 15:137–140
    [Google Scholar]
  6. Costerton J. W., Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322
    [Google Scholar]
  7. Coutinho P. M., Deleury E., Davies G. J., Henrissat B. 2003; An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328:307–317
    [Google Scholar]
  8. Davey M. E., Caiazza N. C., O'Toole G. A. 2003; Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036
    [Google Scholar]
  9. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298
    [Google Scholar]
  10. de Lorenzo V., Timmis K. N. 1994; Analysis and construction of stable phenotypes in gram-negative bacteria with Tn 5 - and Tn 10 -derived minitransposons. Methods Enzymol 235:386–405
    [Google Scholar]
  11. Dubois M., Gilles K. A., Hamilton J. K., Rebers P. A., Smith F. 1956; Colorimetric method for determination of sugars and related substances. Anal Biochem 28:350–356
    [Google Scholar]
  12. Fournet B., Strecker G., Leroy Y., Montreuil J. 1981; Gas-liquid chromatography and mass-spectrometry of methylated and acetylated methylglycosides: application to the structural analysis of glycoprotein glycans. Anal Biochem 116:489–502
    [Google Scholar]
  13. Hardalo C., Edberg S. C. 1997; Pseudomonas aeruginosa : assessment of risk from drinking water. Crit Rev Microbiol 23:47–75
    [Google Scholar]
  14. Harshey R. M. 2003; Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273
    [Google Scholar]
  15. Heydorn A., Nielsen A. T., Hentzer M., Sternberg C., Givskov M., Ersbøll B. K., Molin S. 2000; Quantification of biofilm structures by the novel computer program comstat. Microbiology 146:2395–2407
    [Google Scholar]
  16. Hoiby N. 1993; Cystic fibrosis and endobronchial Pseudomonas infection. Curr Opin Pediatr 5:247–254
    [Google Scholar]
  17. Klausen M., Aaes-Jorgensen A., Molin S., Tolker-Nielsen T. 2003a; Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50:61–68
    [Google Scholar]
  18. Klausen M., Heydorn A., Ragas P., Lambertsen L., Aaes-Jorgensen A., Molin S., Tolker-Nielsen T. 2003b; Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48:1511–1524
    [Google Scholar]
  19. Kohler T., Curty L. K., Barja F., van Delden C., Pechere J. C. 2000; Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182:5990–5996
    [Google Scholar]
  20. Lacroix J. M., Tempete M., Menichi B., Bohin J. P. 1989; Molecular cloning and expression of a locus ( mdoA ) implicated in the biosynthesis of membrane-derived oligosaccharides in Escherichia coli . Mol Microbiol 3:1173–1182
    [Google Scholar]
  21. Lacroix J.-M., Loubens I., Tempête M., Menichi B., Bohin J.-P. 1991; The mdoA locus of Escherichia coli consists of an operon under osmotic control. Mol Microbiol 5:1745–1753
    [Google Scholar]
  22. Lequette Y., Greenberg E. P. 2005; Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37–44
    [Google Scholar]
  23. Loubens I., Debarbieux L., Bohin A., Lacroix J.-M., Bohin J.-P. 1993; Homology between a genetic locus ( mdoA ) involved in the osmoregulated biosynthesis of periplasmic glucans in Escherichia coli and a genetic locus ( hrpM ) controlling pathogenicity of Pseudomonas syringae . Mol Microbiol 10:329–340
    [Google Scholar]
  24. Mah T. F., Pitts B., Pellock B., Walker G. C., Stewart P. S., O'Toole G. A. 2003; A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310
    [Google Scholar]
  25. Mahajan-Miklos S., Tan M.-W., Rahme L. G., Ausubel F. M. 1999; Molecular mechanisms of bacterial virulence elucidated using Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96:47–56
    [Google Scholar]
  26. Mukhopadhyay P., Williams J., Mills D. 1988; Molecular analysis of a pathogenicity locus in Pseudomonas syringae pv. syringae . J Bacteriol 170:5479–5488
    [Google Scholar]
  27. O'Toole G. A., Kolter R. 1998; Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a generic analysis. Mol Microbiol 28:449–461
    [Google Scholar]
  28. Parente J. P., Cardon P., Leroy Y., Montreuil J., Fournet B., Ricard G. 1985; A convenient method for methylation of glycoproteins glycans in small amounts by using lithium methylsulfinyl carbanion. Carbohydr Res 141:41–47
    [Google Scholar]
  29. Rahme L. G., Ausubel F. M., Cao H., Drenkard E., Goumnerov B. C., Lau G. W., Mahajan-Miklos S., Plotnikova J., Tan M.-W. other authors 2000; Plants and animals share functional common bacterial virulence factors. Proc Natl Acad Sci U S A 97:8815–8821
    [Google Scholar]
  30. Schuster M., Lostroh C. P., Ogi T., Greenberg E. P. 2003; Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079
    [Google Scholar]
  31. Schwartz T., Volkmann H., Kirchen S., Kohnen W., Schon-Holz K., Jansen B., Obst U. 2006; Real-time PCR detection of Pseudomonas aeruginosa in clinical and municipal wastewater and genotyping of the ciprofloxacin-resistant isolates. FEMS Microbiol Ecol 57:158–167
    [Google Scholar]
  32. Schweizer H. P. 1991; Escherichia–Pseudomonas shuttle vectors derived from pUC18/19. Gene 97:109–121
    [Google Scholar]
  33. Singh P. K., Schaefer A. L., Parsek M. R., Moninger T. O., Welsh M. J., Greenberg E. P. 2000; Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764
    [Google Scholar]
  34. Smith R. S., Iglewski B. H. 2003; P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6:56–60
    [Google Scholar]
  35. Spiers A. J., Buckling A., Rainey P. B. 2000; The causes of Pseudomonas diversity. Microbiology 146:2345–2350
    [Google Scholar]
  36. Stahl B., Steup M., Karas M., Hillenkamp F. 1991; Analysis of neutral oligosaccharides by matrix-assisted laser desorption/ionization mass spectrometry. Anal Chem 63:1463–1466
    [Google Scholar]
  37. Talaga P., Fournet B., Bohin J.-P. 1994; Periplasmic glucans of Pseudomonas syringae pv. syringae. J Bacteriol 176:6538–6544
    [Google Scholar]
  38. Talaga P., Cogez V., Wieruszeski J. M., Sthal B., Lemoine J., Lippens G., Bohin J. P. 2002; Osmoregulated periplasmic glucans of the free-living photosynthetic bacterium Rhodobacter sphaeroides . Eur J Biochem 269:2464–2472
    [Google Scholar]
  39. Taylor B. L., Koshland D. E. Jr 1974; Reversal of flagellar rotation in monotrichous and peritrichous bacteria: generation of changes in direction. J Bacteriol 119:640–642
    [Google Scholar]
  40. Therisod H., Weissborn A. C., Kennedy E. P. 1986; An essential function for acyl carrier protein in the biosynthesis of membrane-derived oligosaccharides of Escherichia coli . Proc Natl Acad Sci U S A 83:7236–7240
    [Google Scholar]
  41. Woodcock D. M., Crowther P. J., Doherty J., Jefferson S., DeCruz E., Noyer-Weidner M., Smith S. S., Michael M. Z., Graham M. W. 1989; Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17:3469–3478
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/008953-0
Loading
/content/journal/micro/10.1099/mic.0.2007/008953-0
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