To settle or to move? The interplay between two classes of cyclic lipopeptides in the biocontrol strain Pseudomonas CMR12a

Environmental Microbiology

Volumn 16, Issue 7, 2014, Pages 2282-2300

  D'aes, Jolien ^a   Kieu, Nam Phuong ^a   Léclère, Valérie ^b   Tokarski, Caroline ^c   Olorunleke, Feyisara Eyiwumi ^a   De Maeyer, Katrien ^a   Jacques, Philippe ^b   Höfte, Monica ^a   Ongena, Marc ^d  

^a GHENT UNIVERSITY   (Belgium)

^b Cité scientifique   (France)

^c University Lille   (France)

^d UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BASIDIOMYCOTA; PSEUDOMONAS; PSEUDOMONAS TOLAASII;

AGAR; BACTERIAL PROTEIN; CYCLOPEPTIDE; DEPSIPEPTIDE; LIPOPEPTIDE; PEPTIDE SYNTHASE; PHENAZINE DERIVATIVE; TOLAASIN PROTEIN, PSEUDOMONAS TOLAASII;

ARTICLE; BIOFILM; BIOLOGICAL CONTROL AGENT; BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOVEMENT (PHYSIOLOGY); MULTIGENE FAMILY; MUTATION; PSEUDOMONAS;

AGAR; BACTERIAL PROTEINS; BIOFILMS; BIOLOGICAL CONTROL AGENTS; DEPSIPEPTIDES; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPEPTIDES; MOVEMENT; MULTIGENE FAMILY; MUTATION; PEPTIDE SYNTHASES; PEPTIDES, CYCLIC; PHENAZINES; PSEUDOMONAS;

EID: 84903794736     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12462     Document Type: Article

References (69)

1. Andersen, J.B., Koch, B., Nielsen, T.H., Sorensen, D., Hansen, M., Nybroe, O., etal. (2003) Surface motility in Pseudomonas sp. DSS73 is required for efficient biological containment of the root-pathogenic microfungi Rhizoctonia solani and Pythium ultimum. Microbiology 149: 37-46.
2. Bachmann, B.O., and Ravel, J. (2009) In silico prediction of microbial secondary metabolic pathways from DNA sequence data. Methods Enzymol 458: 181-217.
3. Balibar, C.J., Vaillancourt, F.H., and Walsh, C.T. (2005) Generation of D amino acid residues in assembly of arthrofactin by dual condensation/epimerization domains. Chem Biol 12: 1189-1200.
4. Barahona, E., Navazo, A., Yousef-Coronado, F., Aguirre de Carcer, D., Martinez-Granero, F., Espinoza-Urgel, M., etal. (2010) Efficient rhizosphere colonization by Pseudomonas fluorescens f113 mutants unable to form biofilms on abiotic surfaces. Environ Microbiol 12: 3185-3195.
5. Bassarello, C., Lazzaroni, S., Bifulco, G., Lo Cantore, P., Iacobellis, N.S., Riccio, R., etal. (2004) Tolaasins A-E, five new lipodepsipeptides produced by Pseudomonas tolaasii. J Nat Prod 67: 811-816.
6. Batoko, H., d'Exaerde, A.D., Kinet, J.M., Bouharmont, J., Gage, R.A., Maraite, H., and Boutry, M. (1998) Modulation of plant plasma membrane H+-ATPase by phytotoxic lipodepsipeptides produced by the plant pathogen Pseudomonas fuscovaginae. Biochim Biophys Acta-Biomembr 1372: 216-226.
7. Bender, C.L., Alarcon-Chaidez, F., and Gross, D.C. (1999) Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63: 266-292.
8. Brodey, C.L., Rainey, P.B., Tester, M., and Johnstone, K. (1991) Bacterial blotch disease of the cultivated mushroom is caused by an ion channel forming lipodepsipeptide toxin. Mol Plant Microbe Interact 4: 407-411.
9. de Bruijn, I., de Kock, M.J.D., Yang, M., de Waard, P., van Beek, T.A., and Raaijmakers, J.M. (2007) Genome-based discovery, structure prediction and functional analysis of cyclic lipopeptide antibiotics in Pseudomonas species. Mol Microbiol 63: 417-428.
10. Burlinson, P., Studholme, D., Cambray-Young, J., Heavens, D., Rathjen, J., Hodgkin, J., and Preston, G.M. (2013) Pseudomonas fluorescens NZI7 repels grazing by C. elegans, a natural predator. ISME J 7: 1126-1138.
11. Chevreux, B., Wetter, T., and Suhai, S. (1999) Genome sequence assembly using trace signals and additional sequence information. In Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB) 99, Hannover, Germany. pp. 45-56.
12. D'aes, J., De Maeyer, K., Pauwelyn, E., and Höfte, M. (2010) Biosurfactants in plant-Pseudomonas interactions and their importance to biocontrol. Environ Microbiol Rep 2: 359-372.
13. D'aes, J., Hua, G.K.H., De Maeyer, K., Pannecoucque, J., Forrez, I., Ongena, M., etal. (2011) Biological control of Rhizoctonia root rot on bean by phenazine and cyclic lipopeptide producing Pseudomonas CMR12a. Phytopathology 101: 996-1004.
14. Darling, A.C.E., Mau, B., Blattner, F.R., and Perna, N.T. (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403.
15. De Bruijn, I., and Raaijmakers, J.M. (2009) Diversity and functional analysis of LuxR-type transcriptional regulators in cyclic lipopeptide biosynthesis in Pseudomonas fluorescens. Appl Environ Microbiol 75: 4753-4761.
16. De Bruijn, I., de Kock, M.J.D., de Waard, P., van Beek, T.A., and Raaijmakers, J.M. (2008) Massetolide A biosynthesis in Pseudomonas fluorescens. J Bacteriol 190: 2777-2789.
17. De Maeyer, K., D'aes, J., Hua, G.K.H., Perneel, M., Vanhaecke, L., Noppe, H., and Höfte, M. (2011) N-Acylhomoserine lactone quorum-sensing signalling in antagonistic phenazine-producing Pseudomonas isolates from the red cocoyam rhizosphere. Microbiology 157: 459-472.
18. De Maeyer, K., D'aes, J., Hua, G.K.H., Kieu, N.P., and Höfte, M. (2013) N-acetylhomoserine lactone quorum sensing signaling in phenazine and cyclic lipopeptide producing Pseudomonas sp. CMR12a from the red cocoyam rhizosphere. In Molecular Microbial Ecology of the Rhizosphere. de Bruijn, F.J. (ed.). Hoboken, NJ, USA: John Wiley and Sons, pp. 763-774.
19. Delcher, A.L., Bratke, K.A., Powers, E.C., and Salzberg, S.L. (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673-679.
20. Dubern, J.F., Coppoolse, E.R., Stiekema, W.J., and Bloemberg, G.V. (2008) Genetic and functional characterization of the gene cluster directing the biosynthesis of putisolvin I and II in Pseudomonas putida strain PCL1445. Microbiology 154: 2070-2083.
21. Dutta, S., and Podile, A.R. (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36: 232-244.
22. Feil, H., Feil, W.S., Chain, P., Larimer, F., DiBartolo, G., Copeland, A., etal. (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci USA 102: 11064-11069.
23. Finking, R., and Marahiel, M.A. (2004) Biosynthesis of nonribosomal peptides. Annu Rev Microbiol 58: 453-488.
24. Gross, H., and Loper, J.E. (2009) Genomics of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26: 1408-1446.
25. Gross, H., Stockwell, V.O., Henkels, M.D., Nowak-Thompson, B., Loper, J.E., and Gerwick, W.H. (2007) The genomisotopic approach: a systematic method to isolate products of orphan biosynthetic gene clusters. Chem Biol 14: 53-63.
26. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., and 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.
27. Hutchison, M.L., and Johnstone, K. (1993) Evidence for the involvement of the surface active properties of the extracellular toxin tolaasin in the manifestation of brown blotch disease symptoms by Pseudomonas tolaasii on Agaricus bisporus. Physiol Mol Plant Pathol 42: 373-384.
28. Iacobellis, N.S., Lavermicocca, P., Grgurina, I., Simmaco, M., and Ballio, A. (1992) Phytotoxic properties of Pseudomonas syringae pv. syringae toxins. Physiol Mol Plant Pathol 40: 107-116.
29. Jain, D.K., Collinsthompson, D.L., Lee, H., and Trevors, J.T. (1991) A drop-collapsing test for screening surfactant-producing microorganisms. J Microbiol Methods 13: 271-279.
30. Jourdan, E., Henry, G., Duby, F., Dommes, J., Barthelemy, J.P., Thonart, P., and Ongena, M. (2009) Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant Microbe Interact 22: 456-468.
31. Juhas, M., van der Meer, J.R., Gaillard, M., Harding, R.M., Hood, D.W., and Crook, D.W. (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 33: 376-393.
32. King, E.O., Ward, M.K., and Raney, D.E. (1954) Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med 44: 301-307.
33. Kuiper, I., Lagendijk, E.L., Pickford, R., Derrick, J.P., Lamers, G.E.M., Thomas-Oates, J.E., etal. (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51: 97-113.
34. Kunkel, B.N., and Zhongying, C. (2006) Virulence of plant pathogenic bacteria. In Prokaryotes. Dworkin, M., Falkow, F., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E. (eds). New York, NY, USA: Springer, pp. 421-440.
35. Li, W., Rokni-Zadeh, H., De Vleeschouwer, M., Ghequire, M.G.K., Sinnaeve, D., Xie, G.L., etal. (2013) The antimicrobial compound xantholysin defines a new group of Pseudomonas cyclic lipopeptides. PLoS ONE 8: e62946.
36. López, D., Fischbach, M.A., Chu, F., Losick, R., and Kolter, R. (2009) Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc Natl Acad Sci USA 106: 280-285.
37. Lo Cantore, P., Lazzaroni, S., Coraiola, M., Dalla Serra, M., Cafarchia, C., Evidente, A., and Iacobellis, N.S. (2006) Biological characterization of white line-inducing principle (WLIP) produced by Pseudomonas reactans NCPPB1311. Mol Plant Microbe Interact 19: 1113-1120.
38. Maddula, V., Zhang, Z., Pierson, E.A., and Pierson, L.S. (2006) Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30-84. Microb Ecol 52: 289-301.
39. Maddula, V.S., Pierson, E.A., and Pierson, L.S., 3rd (2008) Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on biofilm formation and pathogen inhibition. J Bacteriol 190: 2759-2766.
40. Mavrodi, D.V., Blankenfeldt, W., and Thomashow, L.S. (2006) Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 44: 417-445.
41. Mavrodi, D.V., Peever, T.L., Mavrodi, O.V., Parejko, J.A., Raaijmakers, J.M., Lemanceau, P., etal. (2010) Diversity and evolution of the phenazine biosynthesis pathway. Appl Environ Microbiol 76: 866-879.
42. Mazzola, M., de Bruijn, I., Cohen, M.F., and Raaijmakers, J.M. (2009) Protozoan-induced regulation of cyclic lipopeptide biosynthesis is an effective predation defense mechanism for Pseudomonas fluorescens. Appl Environ Microbiol 75: 6804-6811.
43. Merrit, J.H., Kadouri, D.E., and O'Toole, G.A. (2005) Growing and analyzing static biofilms. In Current Protocols in Microbiology. Coico, R., Kowalik, T., Quarles, J., Stevenson, B., and Taylor, R. (eds). Hoboken, NJ, USA: J. Wiley & Sons, pp. 1B.1.1-1B.1.17.
44. Morikawa, M., Hirata, Y., and Imanaka, T. (2000) A study on the structure-function relationship of lipopeptide biosurfactants. Biochim Biophys Acta-Mol Cell Biol Lipids 1488: 211-218.
45. Mortishire-Smith, R.J., Nutkins, J.C., Packman, L.C., Brodey, C.L., Rainey, P.B., Johnstone, K., and Williams, D.H. (1991) Determination of the structure of an extracellular peptide produced by the mushroom saprotroph Pseudomonas reactans. Tetrahedron 47: 3645-3654.
46. Nutkins, J.C., Mortishire-Smith, R.J., Packman, L.C., Brodey, C.L., Rainey, P.B., Johnstone, K., and Williams, D.H. (1991) Structure determination of tolaasin, an extracellular lipodepsipeptide produced by the mushroom pathogen Pseudomonas tolaasii paine. J Am Chem Soc 113: 2621-2627.
47. Paulsen, I.T., Press, C.M., Ravel, J., Kobayashi, D.Y., Myers, G.S.A., Mavrodi, D.V., etal. (2006) Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 24: 466-466.
48. Pauwelyn, E., Huang, C.-J., Ongena, M., Leclère, V., Jacques, P., Bleyaert, P., etal. (2013) New linear lipopeptides produced by Pseudomonas cichorii SF1-54 are involved in virulence, swarming motility, and biofilm formation. Mol Plant Microbe Interact 26: 585-598.
49. Perneel, M., Heyrman, J., Adiobo, A., De Maeyer, K., Raaijmakers, J.M., De Vos, P., and Hofte, M. (2007) Characterization of CMR5c and CMR12a, novel fluorescent Pseudomonas strains from the cocoyam rhizosphere with biocontrol activity. J Appl Microbiol 103: 1007-1020.
50. Raaijmakers, J.M., de Bruijn, I., and de Kock, M.J.D. (2006) Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol Plant Microbe Interact 19: 699-710.
51. Raaijmakers, J.M., de Bruijn, I., Nybroe, O., and Ongena, M. (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34: 1037-1062.
52. Ramos, I., Dietrich, L.E.P., Price-Whelan, A., and Newman, D.K. (2010) Phenazines affect biofilm formation by Pseudomonas aeruginosa in similar ways at various scales. Res Microbiol 161: 187-191.
53. Rausch, C., Weber, T., Kohlbacher, O., Wohlleben, W., and Huson, D.H. (2005) Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res 33: 5799-5808.
54. Rausch, C., Hoof, I., Weber, T., Wohlleben, W., and Huson, D.H. (2007) Phylogenetic analysis of condensation domains in NRPS sheds light on their functional evolution. BMC Evol Biol 7: 78.
55. Rokni-Zadeh, H., Li, W., Sanchez-Rodriguez, A., Sinnaeve, D., Rozenski, J., Martins, J.C., and De Mot, R. (2012) Genetic and functional characterization of cyclic lipopeptide white-line-inducing principle (WLIP) production by rice rhizosphere isolate Pseudomonas putida RW10S2. Appl Environ Microbiol 78: 4826-4834.
56. Rokni-Zadeh, H., Li, W., Yilma, E., Sanchez-Rodriguez, A., and De Mot, R. (2013) Distinct lipopeptide production systems for WLIP (white line-inducing principle) in Pseudomonas fluorescens and Pseudomonas putida. Environ Microbiol Rep 5: 160-169.
57. Roongsawang, N., Hase, K., Haruki, M., Imanaka, T., Morikawa, M., and Kanaya, S. (2003) Cloning and characterization of the gene cluster encoding arthrofactin synthetase from Pseudomonas sp MIS38. Chem Biol 10: 869-880.
58. Roongsawang, N., Lim, S.P., Washio, K., Takano, K., Kanaya, S., and Morikawa, M. (2005) Phylogenetic analysis of condensation domains in the nonribosomal peptide synthetases. FEMS Microbiol Lett 252: 143-151.
59. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York, NY, USA: Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
60. Schleif, R.F., and Wensink, P.C. (1981) Practical Methods in Molecular Biology. New York, NY, USA: Springer-Verlag.
61. Scholz-Schroeder, B.K., Hutchison, M.L., Grgurina, I., and Gross, D.C. (2001) The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B301D on the basis of sypA and syrB1 biosynthesis mutant analysis. Mol Plant Microbe Interact 14: 336-348.
62. Scholz-Schroeder, B.K., Soule, J.D., and 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 Interact 16: 271-280.
63. Selin, C., Habibian, R., Poritsanos, N., Athukorala, S.N.P., Fernando, D., and de Kievit, T.R. (2010) Phenazines are not essential for Pseudomonas chlororaphis PA23 biocontrol of Sclerotinia sclerotiorum, but do play a role in biofilm formation. FEMS Microbiol Ecol 71: 73-83.
64. Shanks, R.M.Q., Caiazza, N.C., Hinsa, S.M., Toutain, C.M., and O'Toole, G.A. (2006) Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol 72: 5027-5036.
65. Singh, G.M., Vaillancourt, F.H., Yin, J., and Walsh, C.T. (2007) Characterization of SyrC, an aminoacyltransferase shuttling threonyl and chlorothreonyl residues in the syringomycin biosynthetic assembly line. Chem Biol 14: 31-40.
66. Vallet-Gely, I., Novikov, A., Augusto, L., Liehl, P., Bolbach, G., Pechy-Tarr, M., etal. (2010) Association of hemolytic activity of Pseudomonas entomophila, a versatile soil bacterium, with cyclic lipopeptide production. Appl Environ Microbiol 76: 910-921.
67. Verstraeten, N., Braeken, K., Debkumari, B., Fauvart, M., Fransaer, J., Vermant, J., and Michiels, J. (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16: 496-506.
68. Wong, W.C., and Preece, T.F. (1979) Identification of Pseudomonas tolaasi - white line in agar and mushroom tissue block rapid pitting tests. J Appl Bacteriol 47: 401-407.
69. Zerbino, D.R., and Birney, E. (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.