The plant-associated Bacillus amyloliquefaciens strains MEP218 and ARP23 capable of producing the cyclic lipopeptides iturin or surfactin and fengycin are effective in biocontrol of sclerotinia stem rot disease

Journal of Applied Microbiology

Volumn 112, Issue 1, 2012, Pages 159-174

  Alvarez, F ^a   Castro, M ^a   Principe A ^a   Borioli, G ^b   Fischer, S ^a   Mori, G ^a   Jofre E ^a  

^a DEPARTAMENTO DE QUÍMICA   (Argentina)

^b UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Bacillus amyloliquefaciens; Biocontrol; Lipopeptides; Sclerotinia sclerotiorum; Soybean

Indexed keywords

BACTERIOLOGY; DISEASE CONTROL; FUNGI; MASS SPECTROMETRY; STRAIN;

ANTIFUNGAL COMPOUNDS; BACILLUS AMYLOLIQUEFACIENS; CYCLIC LIPOPEPTIDES; FENGYCINS; ITURINS; LIPOPEPTIDES; RP-HPLC; SCLEROTINIA SCLEROTIORUM; SOYBEAN; SUPERNATANTS;

BIOCONTROL;

FENGYCIN; ITURIN A; POLYPEPTIDE ANTIBIOTIC AGENT; SURFACTIN; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; BACTERIAL DISEASE; BACTERIUM; BIOCONTROL AGENT; BIOLOGICAL CONTROL; DISEASE CONTROL; FUNGUS; GERMINATION; INOCULATION; MASS SPECTROMETRY; MORPHOLOGY; PEPTIDE; SOYBEAN; TAXONOMY;

ANTIFUNGAL ACTIVITY; ARTICLE; BACILLUS AMYLOLIQUEFACIENS; BACILLUS ANTHRACIS; BACILLUS CEREUS; BACILLUS MEGATERIUM; BACILLUS PUMILUS; BACILLUS SUBTILIS; BACILLUS THURINGIENSIS; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; DISEASE CONTROL; DISEASE SEVERITY; FUNGAL PLANT DISEASE; GERMINATION; MASS SPECTROMETRY; MORPHOLOGY; NONHUMAN; PARTICLE SIZE; PLANT STEM; PROTECTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SCLEROTINIA SCLEROTIORUM; SOYBEAN; SUPERNATANT;

ARGENTINA;

BACILLUS AMYLOLIQUEFACIENS; BACILLUS SP.; BACILLUS SUBTILIS; GLYCINE MAX; SCLEROTINIA; SCLEROTINIA SCLEROTIORUM;

EID: 83555178407     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.05182.x     Document Type: Article

References (75)

1. Abdullah, M.T., Ali, N.Y. and Suleman, P. (2008) Biological control of Sclerotinia sclerotiorum (Lib.) de Bary with Trichoderma harzianum and Bacillus amyloliquefaciens. Crop Prot 27, 1354-1359.
2. Ahimou, F., Jacques, P. and Deleu, M. (2000) Surfactin and iturin A effects on Bacillus subtilis surface hydrophobicity. Enzym Microb Tech 27, 749-754.
3. Altschul, S., Stephen, F., Madden, T., Shäffer, A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
4. Aranda, F.J., Teruel, J.A. and Ortiz, A. (2005) Further aspects on the hemolytic activity of the antibiotic lipopeptide iturin A. Biochim Biophys Acta 1713, 51-56.
5. Arguelles-Arias, A., Ongena, M., Halimi, B., Lara, Y., Brans, A., Joris, B. and Fickers, P. (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Fact 8, 63-70.
6. Arrebola, E., Jacobs, R. and Korsten, L. (2009) Iturin A is the principal inhibitor in the biocontrol activity of Bacillus amyloliquefaciens PPCB004 against postharvest fungal pathogens. J Appl Microbiol 108, 386-395.
7. Asaka, O. and Shoda, M. (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62, 4081-4085.
8. Athukorala, S.N., Fernando, W.G. and Rashid, K.Y. (2009) Identification of antifungal antibiotics of Bacillus species isolated from different microhabitats using polymerase chain reaction and MALDI-TOF mass spectrometry. Can J Microbiol 55, 1021-1032.
9. Bais, H.P., Fall, R. and Vivanco, J.M. (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134, 307-319.
10. Bolton, M.D., Thomma, B.P.H.J. and Nelson, B.D. (2006) Sclerotinia sclerotiorum (Lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7, 1-16.
11. Carrillo, C., Teruel, J.A., Aranda, F.J. and Ortiz, A. (2003) Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochim Biophys Acta 1611, 91-97.
12. Cazorla, F.M., Romero, D., Pérez-Gracía, A., Lugtenberg, B.J.J., de Vicente, A. and Bloemberg, G. (2007) Isolation and characterization of antagonistic Bacillus subtilis strains from the avocado rhizoplane displaying biocontrol activity. J Appl Microbiol 103, 1950-1959.
13. Chen, Y. and Wang, D. (2005) Two convenient methods to evaluate soybean for resistance to Sclerotinia sclerotiorum. Plant Dis 89, 1268-1272.
14. Chen, X.H., Koumoutsi, A., Scholz, R., Schneider, K., Vater, J., Sussmuth, R., Piel, J. and Borriss, R. (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140, 27-37.
15. Cho, S.J., Lee, S.K., Cha, B.J., Kim, Y.H. and Shin, K.S. (2003) Detection and characterization of the Gloeosporium gloesporioides growth inhibitory compound iturin A from Bacillus subtilis strain KS03. FEMS Microbiol Lett 223, 47-51.
16. Christias, C. and Lockwood, J.L. (1973) Conservation of mycelia constituents in four sclerotium-forming fungi in nutrient deprived conditions. Phytopathology 63, 602-605.
17. Coley-Smith, J.R. and Cooke, R.C. (1971) Survival and germination of fungal sclerotia. Annu Rev Phytopathol 9, 65-92.
18. Cunha, W.G., Tinoco, M.L.P., Pancoti, H.L., Ribeiro, R.E. and Aragao, F.J.L. (2010) High resistance to Sclerotinia sclerotiorum in transgenic soybean plants transformed to express an oxalate decarboxylase gene. Plant Pathol 59, 654-660.
19. Danielson, G.A., Nelson, B.D. and Helms, T.C. (2004) Effect of Sclerotinia stem rot on yield of soybean inoculated at different growth stages. Plant Dis 88, 297-300.
20. Deleu, M., Paquot, M. and Nylander, T. (2008) Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. Biophys J 94, 2667-2679.
21. Donaldson, P.A., Anderson, T., Lane, B.G., Davidson, A.L. and Simmonds, D.H. (2001) Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotinia sclerotiorum. Physiol Mol Plant Pathol 59, 297-307.
22. Fan, B., Chen, X.H., Budiharjo, A., Bleiss, W., Vater, J. and Boriss, R. (2011) Efficient colonization of plant roots by the plant growth promoting bacterium Bacillus amyloliquefaciens FZB42, engineered to express green fluorescent protein. J Biotechnol 151, 303-311.
23. Fehr, W.R., Caviness, C.E., Burmood, D.T. and Pennington, J.S. (1971) Stage development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11, 929-931.
24. Fernando, W.G.D., Nakkeeran, S., Zhang, Y. and Savchuk, S. (2007) Biological control of Sclerotinia sclerotiorum (Lib.) de Bary by Pseudomonas and Bacillus species on canola petals. Crop Prot 26, 100-107.
25. Francius, G., Dufour, S., Deleu, M., Paquot, M., Mingeot-Leclercq, M.P. and Dufrene, Y.F. (2008) Nanoscale membrane activity of surfactins: influence of geometry, charge and hydrophobicity. Biochim Biophys Acta 1778, 2058-2068.
26. Fravel, D.R. (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43, 337-359.
27. Fritze, D. (2004) Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 94, 1245-1248.
28. Gordon, R.E., Haynes, W.C. and Hor-Nay Pang, C. (1973) The Genus Bacillus. Agriculture Handbook no. 427. Washington, DC: United States Department of Agriculture.
29. Grau, C. (1998) Sclerotinia stem rot of soybean. In Soybean Diseases of the North Central Region eds Wyllie, T.D. and Scott, D.H. pp. 56-66. St Paul, MN: American Phytopathological Society.
30. Gu, X.B., Zheng, Z.M., Yu, H.Q., Wang, J., Liang, F.L. and Liu, R.L. (2005) Optimization of medium constituents for a novel lipopeptide production by Bacillus subtilis MO-01 by a response surface method. Proc Biochem 40, 3196-3201.
31. Heerklotz, H. and Seelig, J. (2001) Detergent-like action of the antibiotic peptide surfactin on lipid membranes. Biophys J 81, 1547-1554.
32. Hofemeister, J., Conrad, B., Adler, B., Hofemeister, B., Freesche, J., Kucheryava, N., Steinborn, G., Franke, P. et al. (2004) Genetic analysis of the biosynthesis of non-ribosomal peptide-and poliketide-like antibiotics, iron uptake and biofilm formation by Bacillus subtilis A1/3. Mol Genet Genomics 272, 363-376.
33. Hu, L.B., Shi, Z.Q., Zhang, T. and Yang, Z.M. (2007) Fengycin antibiotics isolated from B-FS01 culture inhibit the growth of Fusarium moniliforme Sheldon ATCC 38932. FEMS Microbiol Lett 272, 91-98.
34. Idriss, E.E., Makarewicz, O., Farouk, A., Rosner, K., Greiner, R., Bochow, H., Richter, T. and Borriss, R. (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148, 2097-2109.
35. Joshi, R. and McSpadden Gardener, B.B. (2006) Identification and characterization of novel genetic markers associated with biological control activities in Bacillus subtilis. Phytopathology 96, 145-154.
36. Joshi, S., Bharucha, Ch. and Desai, A.J. (2007) Production of biosurfactant and antifungal compound by fermented food isolate Bacillus subtilis 20B. Biores Technol 99, 4603-4608.
37. Kim, P.I., Bai, H., Bai, D., Chae, H., Chung, S., Kim, Y., Park, R. and Chi, Y.T. (2004) Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol 97, 942-949.
38. Kita, N., Ohya, T., Uekusa, H., Nombra, K., Manago, M. and Shoda, M. (2005) Biological control of damping-off of tomato seedlings and cucumber Phomopsis root rot by Bacillus subtilis RB14-C. Jpn Agric Res Q 39, 109-114.
39. Koumoutsi, A., Chen, X.H., Henne, A., Liesegang, H., Hitzeroth, G., Franke, P., Vater, J. and Borriss, R. (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186, 1084-1096.
40. Kunst, F., Ogasawara, N., Mozser, I., Albertini, A.M., Alloni, G., Azebedo, V., Bertero, M.G., Bessieres, P., Bolotin, A. and Borchert, A.S. et al. (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249-256.
41. Maget-Dana, R. and Peypoux, F. (1994) Iturins, a special class of pore-forming lipopeptides: biological and physicochemical properties. Toxicology 87, 151-174.
42. Maget-Dana, R., Thimon, L., Peypoux, F. and Ptak, M. (1992) Surfactin/iturin A interactions may explain the synergistic effect of surfactin on the biological properties of iturin A. Biochimie 74, 1047-1051.
43. Mansilla, M.C. and De Mendoza, D. (1997) L-Cysteine biosynthesis in Bacillus subtilis: identification, sequencing, and functional characterization of the gene coding for phosphoadenylylsufate sulfotransferase. J Bacteriol 179, 976-981.
44. Menendez, A.B. and Godeas, A. (1998) Biological control of Sclerotinia sclerotiorum attacking soybean plants. Degradation of the cell walls of this pathogen by Trichoderma harzianum (BAFC 742). Mycopathologia 142, 153-160.
45. Mootz, H.D., Finking, R. and Marahiel, M.A. (2001) 4′-Phosphopantetheine transfer in primary and secondary metabolism of Bacillus subtilis. J Biol Chem 276, 37289-37298.
46. Moyne, A.L., Cleveland, T.E. and Tuzun, S. (2004) Molecular characterization and analysis of the operon encoding the antifungal lipopeptide bacillomycin D. FEMS Microbiol Lett 234, 43-49.
47. Mueller, D.S., Dorrance, A.E., Derksen, R.C., Ozkan, E., Kurle, J.E., Grau, C.R., Gaska, J.M., Hartman, G.L. et al. (2002) Efficacy of fungicides on Sclerotinia sclerotiorum and their potential for control of Sclerotinia stem rot on soybean. Plant Dis 86, 26-31.
48. Murherjee, A.K. and Das, K. (2005) Correlation between diverse cyclic lipopeptides production and regulation of growth and substrate utilization by Bacillus subtilis strains in a particular habitat. FEMS Microbiol Ecol 54, 479-489.
49. Nagórska, K., Bikowski, M. and Obuchowski, M. (2007) Multicelluar behaviour and production of a wide variety of toxic substances support usage of Bacillus subtilis as a powerful biocontrol agent. Acta Biochim Polon 54, 495-508.
50. Nelson, P.E., Toussoun, T.A. and Marasan, W.F.O. (1983) Fusarium species: An Illustrated Manual for Identification. PA: Pennsylvania State University Press.
51. Ongena, M. and Jacques, P. (2007) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16, 115-125.
52. Priest, F.G., Goodfellow, M., Shute, L.A. and Berkeley, R.C.W. (1987) Bacillus amyloliquefaciens sp. nov., nom. rev. Int J Syst Bacteriol 37, 69-71.
53. Principe, A., Alvarez, F., Castro, M., Zacchi, L., Fischer, S., Mori, G. and Jofré, E. (2007) Biocontrol and PGPR features in native strains isolated from saline soils of Argentina. Curr Microbiol 55, 314-322.
54. Romero, D., de Vicente, A., Rakotoaly, R.H., Dufour, S.E., Veening, J.W., Arrebola, E., Cazorla, F.M., Kuipers, O.P., Paquot, M. and Pérez-García, A. (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant Microbe Interact 20, 430-440.
55. del Rio, L.E., Martinson, C.A. and Yang, X.B. (2002) Biological control of sclerotinia stem rot of soybean with Sporidesmium sclerotivorum. Plant Dis 86, 999-1004.
56. SAGyP (2007) Secretaría de Agricultura, Ganadería y Pesca de la Nación, La Agricultura en la Argentina, Ministerio de Economía. Argentina: Buenos Aires.
57. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
58. Sieber, S. and Marahiel, M. (2005) Molecular mechanisms underlying nonribosomal peptide synthesis: approaches to new antibiotics. Chem Rev 105, 715-738.
59. Snook, M.E., Mitchell, T., Hinton, D.M. and Bacon, C.W. (2009) Isolation and characterization of Leu7-surfactin from the endophytic bacterium Bacillus mojavensis RRC 101, a biocontrol agent for Fusarium verticillioides. Agric Food Chem 57, 4287-4292.
60. Souto, G.I., Correa, O.S., Montecchia, M.S., Kerber, N.L., Pycher, N.L., Bachur, M. and García, A.F. (2004) Genetic and functional characterization of a Bacillus sp. strain excreting surfactin and antifungal metabolites partially identified as iturin-like compounds. J Appl Microbiol 97, 1247-1256.
61. Stein, T. (2005) Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol 56, 845-857.
62. Steller, S., Vollenbroich, D., Leenders, F., Stein, T., Conrad, B., Hofmeister, J., Jacques, P., Thonart, P. et al. (1999) Structural and functional organization of the fengycin synthetases multienzyme system from Bacillus subtilis b213 and A1/3. Chem Biol 6, 31-41.
63. Tapi, A., Chollet-Imbert, M., Scherens, B. and Jacques, P. (2010) New approach for the detection of non-ribosomal peptide synthetase genes in Bacillus strains by polymerase chain reaction. Appl Microbiol Biotechnol 85, 1521-1531.
64. Tendulkar, S.R., Saikumari, Y.K., Patel, V., Raghotama, S., Munshi, T.K., Balaram, P. and Chatoo, B.B. (2007) Isolation, purification and characterization of an antifungal molecule produced by Bacillus licheniformis BC98, and its effect on phytopathogen Magnaporthe grisea. J Appl Microbiol 103, 2331-2339.
65. Thimon, L., Peypoux, F., Maget-Dana, R., Roux, B. and Michel, G. (1992) Interactions of bioactive lipopeptides, iturin A and surfactin from Bacillus subtilis. Biotechnol Appl Biochem 16, 144-151.
66. Touré, Y., Ongena, M., Jacques, P., Guiro, A. and Thonart, P. (2004) Role of lipopeptide produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96, 1151-1160.
67. Tsuge, K., Akiyama, T. and Shoda, M. (2001) Cloning, sequencing and characterization of the iturin a operon. J Bacteriol 183, 6265-6273.
68. Vater, J., Kablitz, B., Wilde, C., Franke, P., Mehta, N. and Cameotra, S.S. (2002) Matrix-assisted laser desorption ionization-time of flight mass spectrometry of lipopeptide biosurfactants in whole cells and culture filtrates of Bacillus subtilis C-1 isolated from petroleum sludge. Appl Environ Microbiol 68, 6210-6219.
69. Wattiau, P., Renard, M.E., Ledent, P., Debois, V., Blackman, G. and Agathos, S.N. (2001) A PCR test to identify Bacillus subtilis and closely related species and its application to the monitoring of wastewater biotreatment. Appl Microbiol Biotechnol 56, 816-819.
70. Whipps, J.M. (1987) Effect of media on growth and interactions between a range of soil-borne glasshouse pathogens and antagonistic fungi. New Phytol 107, 127-142.
71. Whipps, J.M., Sreenivasaprasad, S., Muthumeenakshi, S., Rogers, C.W. and Challen, M.P. (2008) Use of Coniothyrium minitans as a biocontrol agent and some molecular aspects of sclerotial mycoparasitism. Eur J Plant Pathol 121, 323-330.
72. Willis, A.T. and Gowland, G. (1960) Egg-yolk reactions of Pseudomonas species. Nature 187, 432-433.
73. Wrather, J.A., Anderson, T.R., Arsyad, D.M., Tan, Y., Ploper, L.D., Porta-Puglia, A., Ram, H.H. and Yorinori, J.T. (2001) Soybean disease loss estimates for the top ten soybean-producing countries in 1998. Can J Plant Pathol 23, 115-121.
74. Zeigler, D. (2003) Gene sequences useful for predicting relatedness of whole genomes in bacteria. Int J Syst Evol Microbiol 53, 1893-1900.
75. Zhang, J.X. and Xue, A.G. (2010) Biocontrol of sclerotinia stem rot (Sclerotinia sclerotiorum) of soybean using novel Bacillus subtilis strain SB24 under control conditions. Plant Pathol 59, 382-391.