New linear lipopeptides produced by pseudomonas cichorii SF1-54 are involved in virulence, swarming motility, and biofilm formation

Molecular Plant-Microbe Interactions

Volumn 26, Issue 5, 2013, Pages 585-598

  Pauwelyn, Ellen ^a,b   Huang, Chien Jui ^a   Ongena, Marc ^c   Leclère, Valérie ^d   Jacques, Philippe ^d   Bleyaert, Peter ^b   Budzikiewicz, Herbert ^e   Schäfer, Mathias ^e   Höfte, Monica ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Inagro Vzw ^*  (Belgium)

^c UNIVERSITY OF LIÈGE   (Belgium)

^d Université de Lille 1 Sciences et Technologies   (France)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPEPTIDE;

ARTICLE; BIOFILM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PSEUDOMONAS; VIRULENCE;

BIOFILMS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; LIPOPEPTIDES; PSEUDOMONAS; VIRULENCE;

LACTUCA; PSEUDOMONAS CICHORII;

EID: 84875990918     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-11-12-0258-R     Document Type: Article

References (78)

1. Ansari, M. Z., Yadav, G., Gokhale, R. S., and Mohanty, D. 2004. NRPSPKS: a knowledge-based resource for analysis of NRPS/PKS megasynthases. Nucleic Acids Res. 32:405-413.
2. Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., Meyer, F., Olsen, G. J., Olson, R., Osterman, A. L., Overbeek, R. A., McNeil, L. K., Paarmann, D., Paczian, T., Parrello, B., Pusch, G. D., Reich, C., Stevens, R., Vassieva, O., Vonstein, V., Wilke, A., and Zagnitko, O. 2008. The RAST server: Rapid annotations using subsystems technology. BMC Genomics 9:75.
3. Bachmann, B. O., and Ravel, J. 2009. Methods for In silico prediction of microbial secondary metabolic pathways from DNA sequence data. Methods Enzymol. 458:181-217.
4. 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.
5. Ballio, A., Barra, D., Bossa, F., Collina, A., Grgurina, I., Marino, G., Moneti, G., Paci, M., Pucci, P., Segre, A., and Simmaco, M. 1991. Syringopeptins, new phytotoxic lipodepsipeptides of Pseudomonas syringae pv. syringae. FEBS (Fed. Eur. Biochem. Soc.) Lett. 291:109-112.
6. Ballio, A., Bossa, F., Di Giorgio, D., Ferranti, P., Paci, M., Pucci, P., Scaloni, A., Segre, A., and Strobel, G.A.1994. Novel bioactive lipodepsipeptides from Pseudomonas syringae-The pseudomycins. FEBS (Fed. Eur. Biochem. Soc.) Lett. 355:96-100.
7. Bender, C. L., and Scholz-Schroeder, B. K. 2004. New insights into the biosynthesis, mode of action, and regulation of syringomycin, syringopeptin and coronatine. Kluwer Academic Press, Dordrecht, The Netherlands.
8. 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.
9. Berti, A. D., Greve, N. J., Christensen, Q. H., and Thomas, M. G. 2007. Identification of a biosynthetic gene cluster and the six associated lipopeptides involved in swarming motility of Pseudomonas syringae pv. tomato DC3000. J. Bacteriol. 189:6312-6323.
10. Bradbury, J. F. 1986. Guide to Plant Pathogenic Bacteria. Oxford University Press, New York.
11. Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Zafar, N., Zhou, L. W., Liu, J., Yuan, Q. P., Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Van Aken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W. L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X. Y., Bender, C. L., White, O., Fraser, C. M., and Collmer, A. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181- 10186.
12. Burch, A. Y., Shimada, B. K., Browne, P. J., and Lindow, S. E. 2010. Novel high-throughput detection method to assess bacterial surfactant production. Appl. Environ. Microbiol. 76:5363-5372.
13. Burch, A. Y., Shimada, B. K., Mullin, S. W. A., Dunlap, C. A., Bowman, M. J., and Lindow, S. E. 2012. Pseudomonas syringae coordinates production of a motility-enabling surfactant with flagellar assembly. J. Bacteriol. 194:1287-1298.
14. Catara, V. 2007. Pseudomonas corrugata: Plant pathogen and/or biological resource? Mol. Plant Pathol. 8:233-244.
15. Challis, G. L., Ravel, J., and Townsend, C. A. 2000. Predictive, structurebased model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem. Biol. 7:211-224.
16. Cottyn, B., Heylen, K., Heyrman, J., Vanhouteghem, K., Pauwelyn, E., Bleyaert, P., Van Vaerenbergh, J., Höfte, M., De Vos, P., and Maes, M. 2009. Pseudomonas cichorii as the causal agent of midrib rot, an emerging disease of greenhouse-grown butterhead lettuce in Flanders. Syst. Appl. Microbiol. 32:211-225.
17. Cottyn, B., Baeyen, S., Pauwelyn, E., Verbaednert, I., De Vos, P., Bleyaert, P., Höfte, M., and Maes, M. 2011. Development of a real-time PCR assay for Pseudomonas cichorii, the causal agent of midrib rot in greenhouse- grown lettuce, and its detection in irrigating water. Plant Pathol. 60:453-461.
18. Coutte, F., Leclère, V., Bechet, M., Guez, J. S., Lecouturier, D., Chollet- Imbert, M., Dhulster, P., and Jacques, P. 2010. Effect of pps disruption and constitutive expression of srfA on surfactin productivity, spreading and antagonistic properties of Bacillus subtilis 168 derivatives. J. Appl. Microbiol. 109:480-491.
19. 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.
20. Danhorn, T., and Fuqua, C. 2007. Biofilm formation by plant-associated bacteria. Annu. Rev. Microbiol. 61:401-422.
21. Darling, A. E., Mau, B., and Perna, N. T. 2010. progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PloS One 5:e11147. Published online
22. Published online. de Bruijn, I., and Raaijmakers, J. M. 2009. Diversity and functional analysis of LuxR-type transcriptional regulators of cyclic lipopeptide biosynthesis in Pseudomonas fluorescens. Appl. Environ. Microbiol. 75:4753- 4761.
23. 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.
24. 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.
25. Delcher, A. L., Harmon, D., Kasif, S., White, O., and Salzberg, S. L. 1999. Improved microbial gene identification with GLIMMER. Nucleic Acids Res. 27:4636-4641.
26. Dereeper, A., Guiqnon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. 2008. Phylogeny.fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36 (Suppl. 2):W465-W469.
27. 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.
28. Emanuele, M. C., Scaloni, A., Lavermicocca, P., Jacobellis, N. S., Camoni, L., Di Giorgio, D., Pucci, P., Paci, M., Segre, A., and Ballio, A. 1998. Corpeptins, new bioactive lipodepsipeptides from cultures of Pseudomonas corrugata. FEBS (Fed. Eur. Biochem. Soc.) Lett. 433:317-320.
29. Feil, H., Feil, W. S., Chain, P., Larimer, F., DiBartolo, G., Copeland, A., Lykidis, A., Trong, S., Nolan, M., Goltsman, E., Thiel, J., Malfatti, S., Loper, J. E., Lapidus, A., Detter, J. C., Land, M., Richardson, P. M., Kyrpides, N. C., Ivanova, N., and Lindow, S. E. 2005. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 102:11064-11069.
30. Flamand, M. C., Pelsser, S., Ewbank, E., and Maraite, H. 1996. Production of syringotoxin and other bioactive peptides by Pseudomonas fuscovaginae. Physiol. Mol. Plant Pathol. 48:217-231.
31. Fogliano, V., Gallo, M., Vinale, F., Ritieni, A., Randazzo, G., Greco, M., Lops, R., and Graniti, A. 1999. Immunological detection of syringopeptins produced by Pseudomonas syringae pv. lachrymans. Physiol. Mol. Plant Pathol. 55:255-261.
32. Fuchs, R., and Buzikiewicz, H. 2001. Rearrangement reactions in the electrospray ionization mass spectrometry of pyoverdins. Int. J. Mass Spectrom. 210/211:603-612.
33. Grgurina, I., Mariotti, F., Fogliano, V., Gallo, M., Scaloni, A., Iacobellis, N. S., Lo Cantore, P., Mannina, L., Castelli, V. V., Greco, M. L., and Graniti, A. 2002. A new syringopeptin produced by bean strains of Pseudomonas syringae pv. syringae. Biochim. Biophys. Acta 1597:81- 89.
34. Grgurina, I., Bensaci, M., Pocsfalvi, G., Mannina, L., Cruciani, O., Fiore, A., Fogliano, V., Sorensen, K. N., and Takemoto, J. Y. 2005. Novel cyclic lipodepsipeptide from Pseudomonas syringae pv. lachrymans strain 508 and syringopeptin antimicrobial activities. Antimicrob. Agents Chemother. 49:5037-5045.
35. Grogan, R. G.,, Misaghi, I. J., Kimble, K. A., Greathead, A. S., Ririe, D., and Bardin, R. 1977. Varnish spot, destructive disease of lettuce in California caused by Pseudomonas cichorii. Phytopathology 67:957-960.
36. Gross, D. C. 1985. Regulation of syringomycin synthesis in Pseudomonas syringae pv. syringae and defined conditions for its production. J. Appl. Bacteriol. 58:167-174.
37. Henry, G., Deleu, M., Jourdan, E., Thonart, P., and Ongena, M. 2011. The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defense responses. Cell. Microbiol. 13:1824-1837.
38. Hikichi, Y., Suzuki, K., Toyoda, K., Horikoshi, M., Hirooka, T., and Okuno, T. 1998. Successive observation of growth and movement of genetically lux-marked Pseudomonas cichorii and the response of host tissues in the same lettuce leaf. Ann. Phytopathol. Soc. Jpn. 64:519- 525.
39. Hildebrand, P. D., Braun, P. G., McRae, K. B., and Lu, X. 1998. Role of the biosurfactant viscosin in broccoli head rot caused by a pectolytic strain of Pseudomonas fluorescens. Can. J. Plant Pathol. 20:296-303.
40. Hoang, T. T., Karkhoff-Schwiezer, R. R., Kutchma, A. J., and Schweizer, H. P. 1998. A broad-host-range Flp-FRT recombination system for sitespecific excision of chromosomally-located DNA sequences: Application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
41. Hojo, H., Koyanagi, M., Tanaka, M., Kajihara, S., Ohnishi, K., Kiba, A., and Hikichi, Y. 2008. The hrp genes of Pseudomonas cichorii are essential for pathogenicity on eggplant but not on lettuce. Microbiology 154:2920-2928.
42. Hu, F. P., Young, J. M., and Fletcher, M. J. 1998. Preliminary description of biocidal (syringomycin) activity in fluorescent plant pathogenic Pseudomonas species. J. Appl. Microbiol. 85:365-371.
43. Hutchison, M. L., and Gross, D. C. 1997. Lipopeptide phytotoxins produced by Pseudomonas syringae pv. syringae: Comparison of the biosurfactant and ion channel-forming activities of syringopeptin and syringomycin. Mol. Plant-Microbe Interact. 10:347-354.
44. Hutchison, M. L., Tester, M. A., and Gross, D. C. 1995. Role of biosurfactant and ion channel-forming activities of syringomycin in transmembrane ion flux-A model for the mechanism of action in the plantpathogen interaction. Mol. Plant-Microbe Interact. 8:610-620.
45. Isogai, A., Iguchi, H., Nakayama, J., Kusai, A., Takemoto, J. Y., and Suzuki, A. 1995. Structural analysis of new syringopeptins by tandem massspectrometry Biosci. Biotechnol. Biochem. 59:1374-1376.
46. Jagger, I. C. 1914. A bacterial leaf spot disease of celery. (Abstr.) Phytopathology 4:395.
47. Jones, J. B., Raju, B. C., and Engelhard, A. W. 1984. Effects of temperature and leaf wetness on development of bacterial spot of geranium and chrysanthemum incited by Pseudomonas cichorii. Plant Dis. 68:248- 251.
48. Kajihara, S., Hojo, H., Koyanagi, M., Tanaka, M., Mizumoto, H., Ohnishi, K., Kiba, A., and Hikichi, Y. 2012. Implication of hrpW in virulence of Pseudomonas cichorii. Plant Pathol. 61:355-363.
49. Kang, H. J., and Gross, D. C. 2005. Characterization of a resistance-nodulation- cell division transporter system associated with the syr-syp genomic island of Pseudomonas syringae pv. syringae. Appl. Environ. Microbiol. 71:5056-5065.
50. Kiba, A., Sangawa, Y., Ohnishi, K., Yao, N., Park, P., Nakayashiki, H., Tosa, Y., Mayama, S., and Hikichi, Y. 2006. Induction of apoptotic cell death leads to the development of bacterial rot caused by Pseudomonas cichorii. Mol. Plant-Microbe Interact. 19:112-122.
51. Kiba, A., Lee, K. Y., Ohnishi, K., Park, P., Nakayashiki, H., Tosa, Y., Mayama, S., and Hikichi, Y. 2009. Induction of reactive oxygen generation and functional changes in mitochondria and their involvement in the development of bacterial rot in lettuce caused by Pseudomonas cichorii. Physiol. Mol. Plant Pathol. 74:45-54.
52. 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.
53. Kroupitski, Y., Pinto, R., Belausov, E., and Sela, S. 2011. Distribution of Salmonella typhimurium in romaine lettuce leaves. Food Microbiol. 28:990-997.
54. Kruijt, M., Tran, H., and Raaijmakers, J. M. 2009. Functional, genetic and chemical characterization of biosurfactants produced by plant growthpromoting Pseudomonas putida 267. J. Appl. Microbiol. 107:546-556.
55. Kuiper, I., Lagendijk, E. L., Pickford, R., Derrick, J. P., Lamers, G. E. M., Thomas-Oates, J. E., Lugtenberg, B. J. J., and 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. Microbiol. 51:97-113.
56. Kunkel, B. N., and Zhongying, C. 2006. Virulence of Plant Pathogenic Bacteria. Springer, New York.
57. Lavermicocca, P., Iacobellis, N. S., Simmaco, M., and Graniti, A. 1997. Biological properties and spectrum of activity of Pseudomonas syringae pv. syringae toxins. Physiol. Mol. Plant Pathol. 50:129-140.
58. Lazzaroni, S., Evidente, A., and Surico, G. 2003. Toxic metabolites and lipopolysaccharides from Pseudomonas cichorii. Kluwer Academic Publishers, Dordrecht, The Netherlands.
59. 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.
60. Merrit, J. H., Kadouri, D. E., and O'Toole, G. A. 2005. Growing and analyzing static biofilms. Pages 1B.1.1-1B.1.17 in: Current Protocols in Microbiology. R. Coico, T. Kowalik, J. Quarles, B. Stevenson, and R. Taylor, eds. John Wiley and Sons, Chichester, U.K.
61. Pauwelyn, E., Vanhouteghem, K., Cottyn, B., De Vos, P., Maes, M., Bleyaert, P., and Höfte, M. 2011. Epidemiology of Pseudomonas cichorii, the case of lettuce midrib rot. J. Phytopathol. 159:298-305.
62. Quigley, N. B., Mo, Y. Y., and Gross, D. C. 1993. SyrD is required for syringomycin production by Pseudomonas syringae pathovar syringae and is related to a family of ATP-binding secretion proteins. Mol. Microbiol. 9:787-801.
63. 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.
64. 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 (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 34:1037-1062.
65. 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 (TSVM). Nucleic Acids Res. 33:5799-5808.
66. 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.
67. 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.
68. Roongsawang, N., Washio, K., and Morikawa, M. 2011. Diversity of nonribosomal peptide synthetases involved in the biosynthesis of lipopeptide biosurfactants. Int. J. Mol. Sci. 12:141-172.
69. Rottig, M., Medema, M. H., Blin, K., Weber, T., Rausch, C., and Kohlbacher, O. 2011. NRPSpredictor2-a web server for predicting NRPS adenylation domain specificity. Nucleic Acids Res. 39:W362- W367.
70. Sambrook, J., and Russel, D. W. 2001. Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
71. Schaad, N. W., Jones, J. B., and Chun, W. 2001. Laboratory Guide for Identification of Plant Pathogenic Bacteria. American Phytopathological Society Press, St. Paul, MN, U.S.A.
72. 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.
73. Simon, R., Priefer, U., and Puhler, A. 1983. A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in gram-negative bacteria. Nat. Biotechnol. 1:784-791.
74. Turnbull, G. A., Morgan, J. A., Whipps, J. M., and Saunders, J. R. 2001. The role of bacterial motility in the survival and spread of Pseudomonas fluorescens in soil and in the attachment and colonisation of wheat roots. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Ecol. 36:21-31.
75. Vallet-Gely, I., Novikov, A., Augusto, L., Liehl, P., Bolbach, G., Pechy- Tarr, M., Cosson, P., Keel, C., Caroff, M., and Lemaitre, B. 2010. Association of hemolytic activity of Pseudomonas entomophila, a versatile soil bacterium, with cyclic lipopeptide production. Appl. Environ. Microbiol. 76:910-921.
76. Wilk, J. D., and Dye, D. W. 1974. Pseudomonas cichorii causing tomato and celery diseases in New Zealand. N. Z. J. Agric. Res. 17:123-130.
77. Yamamoto, S., Kasai, H., Arnold, D. L., Jackson, R. W., Vivian, A., and Harayama, S. 2000. Phylogeny of the genus Pseudomonas: Intrageneric structure reconstructed from the nucleotide sequence of gyrB and rpoD genes. Microbiology 146:2385-2394.
78. Yu, S.-M., and Lee, Y. H. 2012. First report of Pseudomonas cichorii associated with leaf spot on soybean in South Korea. Plant Dis. 96:142.