1887

Abstract

PCL1445 secretes two cyclic lipopeptides, putisolvin I and putisolvin II, which possess a surface-tension-reducing ability, and are able to inhibit biofilm formation and to break down biofilms of species including . The putisolvin synthetase gene cluster () and its surrounding region were isolated, sequenced and characterized. Three genes, termed , and , were identified and shown to be involved in putisolvin biosynthesis. The gene products encode the 12 modules responsible for the binding of the 12 amino acids of the putisolvin peptide moiety. Sequence data indicate that the adenylation domain of the 11th module prioritizes the recognition of Val instead of Leu or Ile and consequently favours putisolvin I production over putisolvin II. Detailed analysis of the thiolation domains suggests that the first nine modules recognize the form of the amino acid residues while the two following modules recognize the form and the last module the or form, indifferently. The gene, which is located upstream of , shows high similarity to -type regulatory genes and is required for the expression of the cluster. In addition, two genes, and , located downstream of were identified and shown to be involved in putisolvin production or export.

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2008-07-01
2020-04-07
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J.. 1990; Basic local alignment search tool. J Mol Biol215:403–410
    [Google Scholar]
  2. Ansari M. Z., Yadav G., Gokhale R. S., Mohanty D.. 2004; NRPS-PKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res32:405–423
    [Google Scholar]
  3. Anthamatten D., Hennecke H.. 1991; The regulatory status of the FixL-like and Fix-J-like genes in Bradyrhizobium japonicum may be different from that in Rhizobium meliloti. Mol Gen Genet225:38–48
    [Google Scholar]
  4. Bairoch A.. 1993; The PROSITE dictionary of site and patterns in proteins, its current status. Nucleic Acids Res21:3097–3103
    [Google Scholar]
  5. Bender C. L., Alarcon-Chalaidez F., Gross D. C.. 1999; Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev63:266–292
    [Google Scholar]
  6. Cutting S., Mandelstam J.. 1986; The nucleotide sequence and the transcription during sporulation of gerE gene of Bacillus subtilis. J Gen Microbiol132:3013–3024
    [Google Scholar]
  7. Delcher A. L., Harmon D., Kasif S., White O., Salzberg S. L.. 1999; Improved microbial gene identification with GLIMMER. Nucleic Acids Res27:4636–4641
    [Google Scholar]
  8. Ditta G., Stanfield S., Corbin D., Helinski D. R.. 1980; Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A77:7347–7351
    [Google Scholar]
  9. Dubern J.-F., Bloemberg G. V.. 2006; Influence of environmental conditions on putisolvins I and II production in Pseudomonas putida strain PCL1445. FEMS Microbiol Lett263:169–175
    [Google Scholar]
  10. Dubern J.-F., Lagendijk E. L., Lugtenberg B. J. J., Bloemberg G. V.. 2005; The heat shock genes dnaK, dnaJ, and grpE are involved in regulation of putisolvin biosynthesis in Pseudomonas putida PCL1445. J Bacteriol187:5967–5976
    [Google Scholar]
  11. Dubern J.-F., Lugtenberg B. J. J., Bloemberg G. V.. 2006; The ppuI-rsaL-ppuR quorum sensing system regulates biofilm formation of Pseudomonas putida PCL1445 by controlling biosynthesis of the cyclic lipopeptides putisolvin I and II. J Bacteriol188:2898–2906
    [Google Scholar]
  12. Ewing B., Green P.. 1998; Basecalling of automated sequencer traces using PHRED. II. Error probabilities. Genome Res8:186–194
    [Google Scholar]
  13. Ewing B., Hillier L., Wendle M. C., Green P.. 1998; Base-calling of automated sequencer traces using PHRED. I. Accuracy assessment. Genome Res8:175–185
    [Google Scholar]
  14. Feil H., Feil W. S., Chain P., Larimer F., DiBartolo G., Copeland A., Lykidis A., Trong S., Nolan M.. other authors 2005; Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci U S A102:11064–11069
    [Google Scholar]
  15. Fuqua C., Winans S. C., Greenberg E. P.. 1996; Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum sensing transcriptional regulators. Annu Rev Microbiol50:727–751
    [Google Scholar]
  16. Grangemard I., Wallach J., Maget-Dana R., Peypoux F.. 2001; Lichenysin: a more efficient cation chelator than surfactin. Appl Biochem Biotechnol90:199–210
    [Google Scholar]
  17. Guenzi E., Galli G., Grgurina I., Gross D. C., Grandi G.. 1998; Characterization of the syringomycin synthetase gene cluster: a link between prokaryotic and eukaryotic peptide synthetases. J Biol Chem273:32857–32863
    [Google Scholar]
  18. Hamblin M. J., Shaw J. G., Kelly D. J.. 1993; Sequence analysis and interposon mutagenesis of a sensor-kinase (DctS) and response-regulator (DctR) controlling synthesis of the high-affinity C4-dicarboxylate transport system in Rhodobacter capsulatus. Mol Gen Genet237:215–224
    [Google Scholar]
  19. Hanahan D.. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol166:557–580
    [Google Scholar]
  20. Heeb S., Itoh Y., Nishijyo T., Schnider U., Keel C., Wade J., Walsh U., O'Gara F., Haas D.. 2000; Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-associated bacteria. Mol Plant Microbe Interact13:232–237
    [Google Scholar]
  21. Henriksen A., Anthoni U., Nielsen T. H., Sørensen J., Christophersen C., Gajhede M.. 2000; Cyclic lipoundecapeptide tensin from Pseudomonas fluorescens strain 96.578. Acta Crystallogr C56:113–115
    [Google Scholar]
  22. Huber B., Riedel K., Kothe M., Givskov M., Molin S., Eberl L.. 2002; Genetic analysis of function involved in the late stages of biofilm development in Burkolderia cepacia HIII. Mol Microbiol46:411–426
    [Google Scholar]
  23. Hutchison M. L., Tester M. A., Gross D. C.. 1995; Role of biosurfactants and ion-channel-forming activities of syringomycin in transmembrane ion flux – a model for the mechanism of action in the plant-pathogen interaction. Mol Plant Microbe Interact8:610–620
    [Google Scholar]
  24. Jain D. K., Thompson D. L., Lee H., Trevors J. T.. 1991; A drop-collapsing test for screening surfactant-producing microorganisms. J Microbiol Methods13:271–279
    [Google Scholar]
  25. King E. O., Ward M. K., Raney D. E.. 1954; Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med44:301–307
    [Google Scholar]
  26. Kitten T., Kinscherf T. G., McEvoy J. L., Willis D. K.. 1998; A newly identified regulator is required for virulence and toxin production in Pseudomonas syringae. Mol Microbiol28:917–929
    [Google Scholar]
  27. Kleinkauf H., von Döhren H.. 1996; A nonribosomal system of peptide biosynthesis. Eur J Biochem236:335–351
    [Google Scholar]
  28. Kobayashi N., Nishino K., Yamagushi A.. 2001; Novel macrolide-specific ABC-type efflux transporter in Escherichia coli. J Bacteriol183:5639–5644
    [Google Scholar]
  29. Koch B., Nielsen T. H., Sørensen D., Andersen J. B., Christophersen C., Molin S., Givskov M., Sørensen J., Nybroe O.. 2002; Lipopeptide production in Pseudomonas sp. strain DSS73 is regulated by components of sugar beet seed exudates via Gac two-component regulatory system. Appl Environ Microbiol68:4509–4516
    [Google Scholar]
  30. Kuiper I., Bloemberg G. V., Noreen S., Thomas-Oates J. E., Lugtenberg B. J.. 2001; Increased uptake of putrescine in the rhizosphere inhibits competitive root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact14:1096–1104
    [Google Scholar]
  31. Kuiper I., Lagendijk E. L., Pickford R., Derrick J. P., Lamers G. E. M., Thomas-Oates J. E., Lugtenberg B. J. J., Bloemberg G. V.. 2004; Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol51:97–113
    [Google Scholar]
  32. Lindum P. W., Anthoni U., Christophersen C., Eberl L., Molin S., Givskov M.. 1998; N-Acyl-l-homoserine lactone autoinducer control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J Bacteriol180:6384–6388
    [Google Scholar]
  33. Linne U., Doekel S., Marahiel M. A.. 2001; Portability of epimerization domain and role of peptidyl carrier protein on epimerization activity in nonribosomal peptide synthetases. Biochemistry40:15824–15834
    [Google Scholar]
  34. Lugtenberg B. J. J., Kravchenko L. V., Simons M.. 1999; Tomato seed and root exudates sugars: composition, utilization by Pseudomonas biocontrol strain and role in rhizosphere colonization. Environ Microbiol1:439–446
    [Google Scholar]
  35. Lukashin A. V., Borodovsky M.. 1998; GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res26:1107–1115
    [Google Scholar]
  36. Marahiel M. A., Stachelhaus T., Mootz H. D.. 1997; Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev97:2651–2673
    [Google Scholar]
  37. Nakajima A., Sugimoto Y., Yoneyama H., Nakae T.. 2000; Localization of the outer membrane subunit OprM of resistance-nodulation-cell division family multi-component efflux pump in Pseudomonas aeruginosa. J Biol Chem275:30064–30068
    [Google Scholar]
  38. Neu T. R.. 1996; Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev60:151–166
    [Google Scholar]
  39. Nielsen T. H., Christophersen C., Anthoni V., Sørensen J.. 1999; Viscosinamide, a new cyclic depsipeptide with surfactant and antifungal properties produced by Pseudomonas fluorescens DR54. J Appl Microbiol87:80–90
    [Google Scholar]
  40. Nutkins J. C., Mortishire-Smith R. J., Packman L. C., Brodey C. L., Rainey P. B., Johnstone K., Williams D. H.. 1991; Structure determination of tolaasin, an extra-cellular lipodepsipeptide produced by the mushroom pathogen Pseudomonas tolaasii Paine. J Am Chem Soc113:2621–2627
    [Google Scholar]
  41. Pabo C. O., Sauer R. T.. 1992; Transcriptional factors: structural families and principles of DNA recognition. Annu Rev Biochem61:1053–1095
    [Google Scholar]
  42. Parkinson J. S., Kofoid E. C.. 1992; Communication modules in bacterial signaling proteins. Annu Rev Genet26:71–112
    [Google Scholar]
  43. Paulsen I. T., Press C. M., Ravel J., Kobayashi D. Y., Myers G. S. A., Mavrodi D. V., DeBoy R. T., Seshadri R., Ren Q.. other authors 2005; Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol23:873–878
    [Google Scholar]
  44. Peters S. A., van Haarst J. C., Jesse T. P., Woltinge D., Jansen K., Hesselink T., van Staveren M. J., Abma-Henkens M. H. C., Klein-Lankhorst R. M.. 2006; TOPAAS, a tomato and potato assembly assistance system for selection and finishing of bacterial artificial chromosomes. Plant Physiol140:805–817
    [Google Scholar]
  45. Peypoux F., Bonmatin J. M., Wallach J.. 1999; Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol51:553–563
    [Google Scholar]
  46. Pittard J., Camakaris H., Yang J.. 2005; The TyrR regulon. Mol Microbiol55:16–26
    [Google Scholar]
  47. Raaijmakers J. M., de Bruijn I., de Kock J. D.. 2006; Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol Plant Microbe Interact19:699–710
    [Google Scholar]
  48. Roongsawang N., Hase K., Haruki M., Imanaka T., Morikawa M., Kanaya S.. 2003; Cloning and characterization of the gene cluster encoding arthrofactin synthetase from Pseudomonas sp. MIS38. . Chem Biol10:869–880
    [Google Scholar]
  49. Rouquette-Loughlin C. E., Balthazar J. T., Shafer W. M.. 2005; Characterization of the MacA-MacB efflux system in Neisseria gonorrhoeae. J Antimicrob Chemother56:856–860
    [Google Scholar]
  50. Sambrook J., Russell D. W.. 2001; Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  51. Schnider U., Keel C., Voisard C., Defago G., Haas D.. 1995; Tn5-directed cloning of pqq genes from Pseudomonas fluorescens CHAO: mutational inactivation of the genes results in overproduction of the antibiotic pyoluteorin. Appl Environ Microbiol61:3856–3864
    [Google Scholar]
  52. Scholz-Schroeder B. K., Soule J. D., Gross D. C.. 2003; The sypA, sypB and sypC synthetase genes encode twenty-two modules involved in the nonribosomal peptide synthesis of syringopeptin by Pseudomonas syringae pv. syringae B301D. Mol Plant Microbe Interact16:271–280
    [Google Scholar]
  53. Sieber S. A., Marahiel M. A.. 2005; Molecular mechanisms underlying nonribosomal peptide synthesis: approaches to new antibiotics. Chem Rev105:715–738
    [Google Scholar]
  54. Sørensen D., Nielsen T. H., Christophersen C., Sørensen J., Gajhede M.. 2001; Cyclic lipoundecapeptide amphisin from Pseudomonas sp. strain DSS73. Acta Crystallogr C57:1123–1124
    [Google Scholar]
  55. Stachelhaus T., Mootz H. D., Marahiel M. A.. 1999; The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol6:493–505
    [Google Scholar]
  56. Wolk C. P., Cai Y., Panoff J. M.. 1991; Use of a transposon with luciferase as a reporter to identify environmentally responsive genes in a cyanobacterium. Proc Natl Acad Sci U S A88:5355–5359
    [Google Scholar]
  57. Yang J., Hwang J. S., Camakaris H., Irawaty W., Ishihama A., Pittard J.. 2004; Mode of action of the TyrR protein: repression and activation of the tyrP promoter of Escherichia coli. Mol Microbiol52:243–256
    [Google Scholar]
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