1887

Abstract

A role for the outer-membrane-associated LapA protein in early biofilm formation by WCS365 has previously been shown. This paper reports that , a gene located adjacent to the gene, also plays a role in biofilm formation. A mutation in results in a conditional biofilm defect in a static assay – this biofilm phenotype is exacerbated when biofilm formation is assayed in a flow-cell system. Furthermore, a mutation shows a partial defect in the transition from reversible to irreversible attachment, consistent with an early role for the gene product in biofilm formation. LapD is shown to be localized to the inner membrane of . The data show decreased LapA associated with the cell surface, but no apparent change in cytoplasmic levels of this protein or transcription, in a mutant. A model is proposed wherein the role of LapD in biofilm formation is modulating the secretion of the LapA adhesin.

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2006-05-01
2019-10-15
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References

  1. Akiyama, Y. & Ito, K. ( 1985; ). The SecY membrane component of the bacterial protein export machinery: analysis by new electrophoretic methods for integral membrane proteins. EMBO J 4, 3351–3356.
    [Google Scholar]
  2. Aravind, L. & Ponting, C. P. ( 1999; ). The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176, 111–116.[CrossRef]
    [Google Scholar]
  3. Ausubel, F. A., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. ( 1990; ). Current Protocols in Molecular Biology. New York: Wiley Interscience.
  4. Christensen, B. B., Sternberg, C., Andersen, J. B., Palmer, R. J., Jr, Nielsen, A. T., Givskov, M. & Molin, S. ( 1999; ). Molecular tools for study of biofilm physiology. Methods Enzymol 310, 20–42.
    [Google Scholar]
  5. Davey, M. E. & O'Toole, G. A. ( 2000; ). Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64, 847–867.[CrossRef]
    [Google Scholar]
  6. DeFlaun, M. F., Tanzer, A. S., McAteer, A., Marshall, B. & Levy, S. B. ( 1990; ). Development of an adhesion assay and characterization of an adhesion-deficient mutant of Pseudomonas fluorescens. Appl Environ Microbiol 56, 112–119.
    [Google Scholar]
  7. de Weger, L. A., van der Vlugt, C. I., Wijfjes, A. H., Bakker, P. A., Schippers, B. & Lugtenberg, B. ( 1987; ). Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. J Bacteriol 169, 2769–2773.
    [Google Scholar]
  8. Duong, F. & Wickner, W. ( 1999; ). The PrlA and PrlG phenotypes are caused by a loosened association among the translocase SecYEG subunits. EMBO J 18, 3263–3270.[CrossRef]
    [Google Scholar]
  9. Fletcher, M. ( 1996; ). Bacterial attachment in aquatic environments: a diversity of surfaces and adhesion strategies. In Bacterial Adhesion: Molecular and Ecological Diversity, pp. 1–24. Edited by M. Fletcher. New York: Wiley.
  10. Friedman, L. & Kolter, R. ( 2004; ). Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51, 675–690.
    [Google Scholar]
  11. Gal, M., Preston, G. M., Massey, R. C., Spiers, A. J. & Rainey, P. B. ( 2003; ). Genes encoding a cellulosic polymer contribute toward the ecological success of Pseudomonas fluorescens SBW25 on plant surfaces. Mol Ecol 12, 3109–3121.[CrossRef]
    [Google Scholar]
  12. Galperin, M. Y., Nikolskaya, A. N. & Koonin, E. V. ( 2001; ). Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203, 11–21.[CrossRef]
    [Google Scholar]
  13. Garcia, B., Latasa, C., Solano, C., Garcia-del Portillo, F., Gamazo, C. & Lasa, I. ( 2004; ). Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol Microbiol 54, 264–277.[CrossRef]
    [Google Scholar]
  14. Gjermansen, M., Ragas, P., Sternberg, C., Molin, S. & Tolker-Nielsen, T. ( 2005; ). Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol 7, 894–904.[CrossRef]
    [Google Scholar]
  15. Guzman, L. M., Belin, D., Carson, M. J. & Beckwith, J. ( 1995; ). Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177, 4121–4130.
    [Google Scholar]
  16. Hinsa, S. M., Espinosa-Urgel, M., Ramos, J. L. & O'Toole, G. A. ( 2003; ). Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49, 905–918.[CrossRef]
    [Google Scholar]
  17. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J. & Schweizer, H. P. ( 1998; ). A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212, 77–86.[CrossRef]
    [Google Scholar]
  18. Jensen, E. T., Kharazmi, A., Hoiby, N. & Costerton, J. W. ( 1992; ). Some bacterial parameters influencing the neutrophil oxidative burst response to Pseudomonas aeruginosa. APMIS 100, 727–733.[CrossRef]
    [Google Scholar]
  19. Korber, D. R., Lawrence, J. R. & Caldwell, D. E. ( 1994; ). Effect of motility on surface colonization and reproductive success of Pseudomonas fluorescens in dual-dilution continuous culture and batch culture systems. Appl Environ Microbiol 60, 1421–1429.
    [Google Scholar]
  20. Kuchma, S. L., Connolly, J. P. & O'Toole, G. A. ( 2005; ). A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J Bacteriol 187, 1441–1454.[CrossRef]
    [Google Scholar]
  21. Lawrence, J. R., Delaquis, P. J., Korber, D. R. & Caldwell, D. E. ( 1987; ). Behavior of Pseudomonas fluorescens within the hydrodynamic boundary layers of surface microenvironments. Microb Ecol 14, 1–14.[CrossRef]
    [Google Scholar]
  22. Leigh, J. A., Signer, E. R. & Walker, G. C. ( 1985; ). Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A 82, 6231–6235.[CrossRef]
    [Google Scholar]
  23. Liu, M., Gonzalez, J. E., Willis, L. B. & Walker, G. C. ( 1998; ). A novel screening method for isolating exopolysaccharide-deficient mutants. Appl Environ Microbiol 64, 4600–4602.
    [Google Scholar]
  24. Longtine, M. S., McKenzie, A., III, Demarini, D. J., Shah, N. G., Wach, A., Brachat, A., Philippsen, P. & Pringle, J. R. ( 1998; ). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953–961.[CrossRef]
    [Google Scholar]
  25. Marshall, K. C. ( 1979; ). Growth at interfaces. In Strategies of Microbial Life in Extreme Environments, pp. 280–290. Edited by M. Shilo. Berlin: Dahlem Konferenzen.
  26. Matthysse, A. G. & McMahan, S. ( 1998; ). Root colonization by Agrobacterium tumefaciens is reduced in cel, attB, attD, and attR mutants. Appl Environ Microbiol 64, 2341–2345.
    [Google Scholar]
  27. Nunn, D. N. & Lory, S. ( 1993; ). Cleavage, methylation, and localization of the Pseudomonas aeruginosa export proteins XcpT, -U, -V, and -W. J Bacteriol 175, 4375–4382.
    [Google Scholar]
  28. O'Toole, G. A. & Kolter, R. ( 1998a; ). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30, 295–304.[CrossRef]
    [Google Scholar]
  29. O'Toole, G. A. & Kolter, R. ( 1998b; ). Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28, 449–461.[CrossRef]
    [Google Scholar]
  30. O'Toole, G. A., Pratt, L. A., Watnick, P. I., Newman, D. K., Weaver, V. B. & Kolter, R. ( 1999; ). Genetic approaches to the study of biofilms. Methods Enzymol 310, 91–109.
    [Google Scholar]
  31. O'Toole, G. A., Kaplan, H. & Kolter, R. ( 2000; ). Biofilm formation as microbial development. Annu Rev Microbiol 54, 49–79.[CrossRef]
    [Google Scholar]
  32. Pardee, A. B., Jacob, F. & Monod, J. ( 1959; ). The genetic control and cytoplasmic expression of “inducibility” in the synthesis of β-galactosidase in E. coli. J Mol Biol 1, 165–178.[CrossRef]
    [Google Scholar]
  33. Read, R. R. & Costerton, J. W. ( 1987; ). Purification and characterization of adhesive exopolysaccharides from Pseudomonas putida and Pseudomonas fluorescens. Can J Microbiol 33, 1080–1090.[CrossRef]
    [Google Scholar]
  34. Reisner, A., Hoiby, N., Tolker-Nielsen, T. & Molin, S. ( 2005; ). Microbial pathogenesis and biofilm development. Contrib Microbiol 12, 114–131.
    [Google Scholar]
  35. Romling, U. ( 2005; ). Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62, 1234–1246.[CrossRef]
    [Google Scholar]
  36. Ross, P., Mayer, R. & Benziman, M. ( 1991; ). Cellulose biosynthesis and function in bacteria. Microbiol Rev 55, 35–58.
    [Google Scholar]
  37. Sauer, K. & Camper, A. K. ( 2001; ). Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol 183, 6579–6589.[CrossRef]
    [Google Scholar]
  38. Simm, R., Morr, M., Kader, A., Nimtz, M. & Romling, U. ( 2004; ). GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53, 1123–1134.[CrossRef]
    [Google Scholar]
  39. Spiers, A. J., Bohannon, J., Gehrig, S. M. & Rainey, P. B. ( 2003; ). Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50, 15–27.[CrossRef]
    [Google Scholar]
  40. Tal, R., Wong, H. C., Calhoon, R. & 11 other authors ( 1998; ). Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180, 4416–4425.
    [Google Scholar]
  41. 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 A 76, 4350–4354.[CrossRef]
    [Google Scholar]
  42. van Loosdrecht, M. C., Lyklema, J., Norde, W. & Zehnder, A. J. B. ( 1990; ). Influence of interfaces on microbial activity. Microbiol Rev 54, 75–87.
    [Google Scholar]
  43. Webb, J. S., Givskov, M. & Kjelleberg, S. ( 2003; ). Bacterial biofilms: prokaryotic adventures in multicellularity. Curr Opin Microbiol 6, 578–585.[CrossRef]
    [Google Scholar]
  44. Zobell, C. E. ( 1943; ). The effects of solid surfaces upon bacterial activity. J Bacteriol 46, 39–56.
    [Google Scholar]
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