1887

Abstract

This study demonstrates that attachment of the marine bacterium to the cellulose-containing surface of the green alga is mediated by a mannose-sensitive haemagglutinin (MSHA-like) pilus. We have identified an MSHA pilus biogenesis gene locus in , termed , which shows significant homology, with respect to its genetic characteristics and organization, to the MSHA pilus biogenesis gene locus of . Electron microscopy studies revealed that wild-type cells express flexible pili peritrichously arranged on the cell surface. A mutant (SM5) with a transposon insertion in the region displayed a non-piliated phenotype. Using SM5, it has been demonstrated that the MSHA pilus promotes attachment of wild-type cells in polystyrene microtitre plates, as well as to microcrystalline cellulose and to the living surface of . also demonstrated increased pilus production in response to cellulose and its monomer constituent cellobiose. The MSHA pilus thus functions as a determinant of attachment in , and it is proposed that an understanding of surface sensing mechanisms displayed by will provide insight into specific ecological interactions that occur between this bacterium and higher marine organisms.

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2006-10-01
2024-11-14
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References

  1. Alm R. A, Mattick J. S. 1997; Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa . Gene 192:89–98 [CrossRef]
    [Google Scholar]
  2. Altschul S. F, Gish W, Miller W, Meyers E. W, Lipman D. J. 1990; Basic Local Alignment Search Tool. J Mol Biol 215:403–410 [CrossRef]
    [Google Scholar]
  3. Bagdasarian M, Lurz R, Ruckert B, Franklin F. C, Bagdasarian M. M, Frey J, Timmis K. N. 1981; Specific-purpose plasmid cloning vectors. II. Broad host range, high copy number, RSF1010-derived vectors, and a host–vector system for gene cloning in Pseudomonas . Gene 16:237–247 [CrossRef]
    [Google Scholar]
  4. Bayer E, Kenig R, Lamed R. 1983; Adherence of Clostridium thermocellum to cellulose. J Bacteriol 156:818–827
    [Google Scholar]
  5. Boyd J. M. 2000; Localization of the histidine kinase PilS to the poles of Pseudomonas aeruginosa and identification of a localization domain. Mol Microbiol 36:153–162 [CrossRef]
    [Google Scholar]
  6. Bryers J, Characklis W. 1982; Processes governing primary biofilm formation. Biotechnol Bioeng 24:2451–2476 [CrossRef]
    [Google Scholar]
  7. Chapman A. R. O. 1979 Biology of Seaweeds: Levels of Organization Baltimore, MD: University Park Press;
    [Google Scholar]
  8. Chiavelli D. A, Marsh J. W, Taylor R. K. 2001; The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67:3220–3225 [CrossRef]
    [Google Scholar]
  9. Cormack B. P, Valdivia R. H, Falkow S. 1996; FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33–38 [CrossRef]
    [Google Scholar]
  10. De Leo G, Patricolo E, D'Ancona-Lunetta G. 1977; Studies on the fibrous components of the test of Ciona intestinalis Linnaes. Cellulose-like polysaccharide. Acta Zoo 58:135–141 [CrossRef]
    [Google Scholar]
  11. de Nys R, Steinberg P, Willemsen P, Dworjanyn S, Gabelish C, King R. 1995; Broad spectrum effects of secondary metabolites from the red alga Delisea pulchra in antifouling assays. Biofouling 8:259–271 [CrossRef]
    [Google Scholar]
  12. Egan S, Thomas T, Holmström C, Kjelleberg S. 2000; Phylogenetic relationship and antifouling activities of bacterial epiphytes from the marine alga Ulva lactuca . Environ Microbiol 2:343–347 [CrossRef]
    [Google Scholar]
  13. Egan S, Holmström C, Kjelleberg S. 2001a; Pseudoalteromonas ulvae sp. nov., a bacterium with antifouling activities isolated from the surface of a marine alga. Int J Syst Evol Microbiol 51:1499–1504
    [Google Scholar]
  14. Egan S, James S, Holmström C, Kjelleberg S. 2001b; Inhibition of algal spore germination by the marine bacterium Pseudoalteromonas tunicata . FEMS Microbiol Ecol 35:67–73 [CrossRef]
    [Google Scholar]
  15. Egan S, James S, Holmström C, Kjelleberg S. 2002a; Correlation between pigmentation and antifouling compounds produced by Pseudoalteromonas tunicata . Environ Microbiol 4:433–442 [CrossRef]
    [Google Scholar]
  16. Egan S, James S, Kjelleberg S. 2002b; Identification and characterization of a putative transcriptional regulator controlling the expression of fouling inhibitors in Pseudoalteromonas tunicata . Appl Environ Microbiol 68:372–378 [CrossRef]
    [Google Scholar]
  17. Gardel C, Mekalanos J. 1996; Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun 64:2246–2255
    [Google Scholar]
  18. Harrison P. 1992; Control of microbial growth and of amphipod gazing by water-soluble compounds from leaves of Zostera marina . Mar Biol 67:25–30
    [Google Scholar]
  19. Hase C. C, Bauer M. E, Finkelstein R. A. 1994; Genetic characterization of mannose-sensitive hemagglutinin (MSHA)-negative mutants of Vibrio cholerae derived by Tn 5 mutagenesis. Gene 150:17–25 [CrossRef]
    [Google Scholar]
  20. Hobbs M, Collie E, Free P, Livingston S, Mattick J. 1993; PilS and PilR, a two component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa . Mol Microbiol 7:669–682 [CrossRef]
    [Google Scholar]
  21. Holmström C., Kjelleberg S. 1999; Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol 30:285–293 [CrossRef]
    [Google Scholar]
  22. Holmström C, Rittschof D, Kjelleberg S. 1992; Inhibition of settlement by larvae of Balanus amphitrite and Ciona intestinalis by a surface-colonizing marine bacterium. Appl Environ Microbiol 58:2111–2115
    [Google Scholar]
  23. Holmström C, James S, Egan S, Kjelleberg S. 1996; Inhibition of common fouling organisms by marine bacterial isolates with special reference to the role of pigmented bacteria. Biofouling 10:251–259 [CrossRef]
    [Google Scholar]
  24. Holmström C, James S, Neilan B, White D, Kjelleberg S. 1998; Pseudoalteromonas tunicata sp. nov., a bacterium that produces antifouling agents. Int J Syst Bacteriol 48:1205–1212 [CrossRef]
    [Google Scholar]
  25. Holmström C, Egan S, Franks A, McCloy S, Kjelleberg S. 2002; Antifouling activities expressed by marine surface associated Pseudoalteromonas species . FEMS Microbiol Ecol 41:47–58 [CrossRef]
    [Google Scholar]
  26. James S, Holmström C, Kjelleberg S. 1996; Purification and characterization of a novel antibacterial protein from the marine bacterium D2. Appl Environ Microbiol 62:2783–2788
    [Google Scholar]
  27. Jonson G, Holmgren J, Svennerholm A. 1991; Identification of a mannose-binding pilus on Vibrio cholerae El Tor. Microb Pathog 11:433–441 [CrossRef]
    [Google Scholar]
  28. Marden P, Tunlid A, Malmcrona-Friberg K, Odham G, Kjelleberg S. 1985; Physiological and morphological changes during short term starvation of marine bacterial isolates. Arch Microbiol 142:326–332 [CrossRef]
    [Google Scholar]
  29. Marsh J. W, Taylor R. K. 1999; Genetic and transcriptional analyses of the Vibrio cholerae mannose-sensitive hemagglutinin type 4 pilus gene locus. J Bacteriol 181:1110–1117
    [Google Scholar]
  30. Martin P, Watson A, McCaul T, Mattick J. 1995; Characterization of a five-gene cluster required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa . Mol Microbiol 16:497–508 [CrossRef]
    [Google Scholar]
  31. Mary A, Mary V, Rittschof D, Nagabhushanam R. 1993; Bacterial–barnacle interaction: potential for using juncellins and antibiotics to alter structure of bacterial communities. J Chem Ecol 19:2155–2167 [CrossRef]
    [Google Scholar]
  32. Mathews C. K, van Holde K. E. 1990 Biochemistry Redwood City, CA: The Benjamin/Cummings Publishing Company;
    [Google Scholar]
  33. Maximilien R, de Nys R, Holmström C, Gram L, Givskov M, Crass K, Kjelleberg S, Steinberg P. 1995; Chemical mediation of bacterial surface colonization by secondary metabolites from red algal Delisea pulchra . Aquat Microb Ecol 15:233–246
    [Google Scholar]
  34. Morand P. C, Tattevin P, Eugene E, Beretti J.-L, Nassif X. 2001; The adhesive property of the type IV pilus-associated component PilC1 of pathogenic Neisseria is supported by the conformational structure of the N-terminal part of the molecule. Mol Microbiol 40:846–856 [CrossRef]
    [Google Scholar]
  35. Neidhardt F, Bloch P, Smith D. 1974; Culture medium for enterobacteria. J Bacteriol 119:736–747
    [Google Scholar]
  36. O'Toole G. A, Kolter R. 1998; Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304 [CrossRef]
    [Google Scholar]
  37. Rao D, Webb J. S, Kjelleberg S. 2005; Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata . Appl Environ Microbiol 71:1729–1736 [CrossRef]
    [Google Scholar]
  38. Rao D, Webb J. S, Kjelleberg S. 2006; Microbial colonization and competition on the marine alga Ulva australis . Appl Environ Microbiol 72:5547–5555 [CrossRef]
    [Google Scholar]
  39. Reese M. 2001; Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comp Chem 26:51–56 [CrossRef]
    [Google Scholar]
  40. Strom M. S, Lory S. 1993; Structure–function and biogenesis of the type IV pili. Annu Rev Microbiol 47:565–596 [CrossRef]
    [Google Scholar]
  41. Taylor C. M, Beresford M, Epton H. A. S, Sigee D. C, Shama G, Andrew P. W, Roberts I. S. 2002; Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J Bacteriol 184:621–628 [CrossRef]
    [Google Scholar]
  42. Tillett D, Neilan B. A. 1999; n -Butanol purification of dye terminator sequencing reactions. Biotechniques 26:606–608 610
    [Google Scholar]
  43. Watnick P. I, Kolter R. 1999; Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol 34:586–595 [CrossRef]
    [Google Scholar]
  44. Watnick P. I, Fullner K. J, Kolter R. 1999; A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol 181:3606–3609
    [Google Scholar]
  45. Zampini M, Canesi L, Betti M, Ciacci C, Tarsi R, Gallo G, Pruzzo C. 2003; Role for mannose-sensitive hemagglutinin in promoting interactions between Vibrio cholerae El Tor and mussel hemolymph. Appl Environ Microbiol 69:5711–5715 [CrossRef]
    [Google Scholar]
  46. Zolfaghar I, Evans D. J, Fleiszig S. M. J. 2003; Twitching motility contributes to the role of pili in corneal infection caused by Pseudomonas aeruginosa . Infect Immun 71:5389–5393 [CrossRef]
    [Google Scholar]
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