Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/amyloliquefaciens

[en] Summary: Some isolates of the Bacillus subtilis/amyloliquefaciens species are known for their plant protective activity against fungal phytopathogens. It is notably due to their genetic potential to form an impressive array of antibiotics including non-ribosomal lipopeptides (LPs). In the work presented here, we wanted to gain further insights into the relative role of these LPs in the global antifungal activity of B.subtilis/amyloliquefaciens. To that end, a comparative study was conducted involving multiple strains that were tested against four different phytopathogens. We combined various approaches to further exemplify that secretion of those LPs is a crucial trait in direct pathogen ward off and this can actually be generalized to all members of these species. Our data illustrate that for each LP family, the fungitoxic activity varies in function of the target species and that the production of iturins and fengycins is modulated by the presence of pathogens. Our data on the relative involvement of these LPs in the biocontrol activity and modulation of their production are discussed in the context of natural conditions in the rhizosphere. © 2014 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology.

Disciplines :

Microbiology

Author, co-author :

Cawoy, H.; Walloon Center for Industrial Microbiology, Gembloux Agro-Bio Tech, University of Liege, Gembloux, Belgium

Debois, Delphine ; Université de Liège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)

Franzil, Laurent ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Bio-industries

De Pauw, Edwin ; Université de Liège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)

Thonart, Philippe ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Bio-industries

Ongena, Marc ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Bio-industries

Language :

English

Title :

Lipopeptides as main ingredients for inhibition of fungal phytopathogens by Bacillus subtilis/amyloliquefaciens

Publication date :

2015

Journal title :

Microbial Biotechnology

ISSN :

1751-7915

eISSN :

1751-7907

Publisher :

John Wiley and Sons

Volume :

Issue :

Pages :

281-295

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 29 June 2015

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Scopus citations^®

220

Scopus citations^®
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213

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192

Bibliography

Angelini, T.E., Roper, M., Kolter, R., Weitz, D.A., and Brenner, M.P. (2009) Bacillus subtilis spreads by surfing on waves of surfactant. Proc Natl Acad Sci USA 106: 18109-18113.
Arguelles-Arias, A., Ongena, M., Halimi, B., Lara, Y., Brans, A., Joris, B., etal. (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Fact 8: 16.
Avis, T.J., and Bélanger, R.R. (2001) Specificity and mode of action of the antifungal fatty acid cis-9-heptadecenoic acid produced by Pseudozyma flocculosa. Appl Environ Microbiol 67: 956-960.
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.
Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., and Vivanco, J.M. (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233-266.
Berendsen, R.L., Pieterse, C.M.J., and Bakker, P.A.H.M. (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17: 478-486.
Cawoy, H., Bettiol, W., Fickers, P., and Ongena, M. (2011) Bacillus-based biological control of plant diseases. In Pesticides in the Modern World - Pesticides Use and Management. Stoytcheva, M. (ed.). Rijeka, Croatia: InTech, pp. 274-302.
Cawoy, H., Mariutto, M., Henry, G., Fisher, C., Vasilyeva, N., Thonart, P., etal. (2014) Plant defense stimulation by natural isolates of Bacillus depends on efficient surfactin production. Mol Plant Microbe Interact 27: 87-100.
Chen, X.H., Koumoutsi, A., Scholz, R., Schneider, K., Vater, J., Süssmuth, R., etal. (2009) Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol 140: 27-37.
D'aes, J., Kieu, N.P., Léclère, V., Tokarski, C., Olorunleke, F.E., De Maeyer, K., etal. (2014) To settle or to move? The interplay between two classes of cyclic lipopeptides in the biocontrol strain Pseudomonas CMR12a. Environ Microbiol 16: 2282-2300.
Debois, D., Ongena, M., Cawoy, H., and De Pauw, E. (2013) MALDI-FTICR MS imaging as a powerful tool to identify paenibacillus antibiotics involved in the inhibition of plant pathogens. J Am Soc Mass Spectrom 24: 1202-1213.
Debois, D., Jourdan, E., Smargiasso, N., Thonart, P., De Pauw, E., and Ongena, M. (2014) Spatiotemporal monitoring of the antibiome secreted by Bacillus biofilms on plant roots using MALDI mass spectrometry imaging. Anal Chem 86: 4431-4438.
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.
Dietel, K., Beator, B., Budiharjo, A., Fan, B., and Borriss, R. (2013) Bacterial traits involved in colonization of Arabidopsis thaliana roots by Bacillus amyloliquefaciens FZB42. Plant Pathol J 29: 59-66.
Eeman, M., Pegado, L., Dufrêne, Y.F., Paquot, M., and Deleu, M. (2009) Influence of environmental conditions on the interfacial organisation of fengycin, a bioactive lipopeptide produced by Bacillus subtilis. J Colloid Interface Sci 329: 253-264.
Falardeau, J., Wise, C., Novitsky, L., and Avis, T.J. (2013) Ecological and mechanistic insights into the direct and indirect antimicrobial properties of Bacillus subtilis lipopeptides on plant pathogens. J Chem Ecol 39: 869-878.
Frey-Klett, P., Burlinson, P., Deveau, A., Barret, M., Tarkka, M., and Sarniguet, A. (2011) Bacterial-fungal interactions: hyphens between agricultural, clinical, environmental, and food microbiologists. Microbiol Mol Biol Rev 75: 583-609.
Hamdache, A., Lamarti, A., Aleu, J., and Collado, I.G. (2011) Non-peptide metabolites from the genus Bacillus. J Nat Prod 74: 893-899.
He, Z., Kisla, D., Zhang, L., Yuan, C., Green-Church, K.B., and Yousef, A.E. (2007) Isolation and identification of a Paenibacillus polymyxa strain that coproduces a novel lantibiotic and polymyxin. Appl Environ Microbiol 73: 168-178.
Hu, L.B., Zhang, T., Yang, Z.M., Zhou, W., and Shi, Z.Q. (2009) Inhibition of fengycins on the production of fumonisin B1 from Fusarium verticillioides. Lett Appl Microbiol 48: 84-89.
Huang, E., and Yousef, A.E. (2012) Draft genome sequence of Paenibacillus polymyxa OSY-DF, which coproduces a lantibiotic, paenibacillin, and polymyxin E1. J Bacteriol 194: 4739-4740.
Jacques, P., Hbid, C., Destain, J., Razafindralambo, H., Paquot, M., De Pauw, E., etal. (1999) Optimization of biosurfactant lipopeptide production from Bacillus subtilis S499 by Plackett-Burman design. Appl Biochem Biotechnol 77-79: 223-233.
Jourdan, E., Henry, G., Duby, F., Dommes, J., Barthélemy, J.P., Thonart, P., etal. (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.
Kinsella, K., Schulthess, C.P., Morris, T.F., and Stuart, J.D. (2009) Rapid quantification of Bacillus subtilis antibiotics in the rhizosphere. Soil Biol Biochem 41: 374-379.
Kirk, W.W., Gachango, E., Schafer, R., and Wharton, P.S. (2013) Effects of in-season crop-protection combined with postharvest applied fungicide on suppression of potato storage diseases caused by Fusarium pathogens. Crop Prot 51: 77-84.
Kurusu, K., Ohba, K., Arai, T., and Fukushima, K. (1987) New peptide antibiotics LI-F03, F04, F05, F07, and F08, produced by Bacillus polymyxa. I. Isolation and characterization. J Antibiot 40: 1506-1514.
Larkin, R.P., and Tavantzis, S. (2013) Use of biocontrol organisms and compost amendments for improved control of soilborne diseases and increased potato production. Am J Potato Res 90: 261-270.
Lee, S.H., Cho, Y.E., Park, S.H., Balaraju, K., Park, J.W., Lee, S.W., etal. (2013) An antibiotic fusaricidin: a cyclic depsipeptide from Paenibacillus polymyxa E681 induces systemic resistance against Phytophthora blight of red-pepper. Phytoparasitica 41: 49-58.
Li, J., and Jensen, S.E. (2008) Nonribosomal biosynthesis of fusaricidins by Paenibacillus polymyxa PKB1 involves direct activation of a d-amino acid. Chem Biol 15: 118-127.
Lugtenberg, B., and Kamilova, F. (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541-556.
McSpadden Gardener, B.B. (2004) Ecology of Bacillus and Paenibacillus spp. in agricultural systems. Phytopathology 94: 1252-1258.
Malfanova, N., Franzil, L., Lugtenberg, B., Chebotar, V., and Ongena, M. (2012) Cyclic lipopeptide profile of the plant-beneficial endophytic bacterium Bacillus subtilis HC8. Arch Microbiol 194: 893-899.
Martin, N.I., Hu, H., Moake, M.M., Churey, J.J., Whittal, R., Worobo, R.W., etal. (2003) Isolation, structural characterization, and properties of mattacin (polymyxin M), a cyclic peptide antibiotic produced by Paenibacillus kobensis M. J Biol Chem 278: 13124-13132.
Mora, I., Cabrefiga, J., and Montesinos, E. (2011) Antimicrobial peptide genes in Bacillus strains from plant environments. Int Microbiol 14: 213-223.
Nasir, M.N., and Besson, F. (2011) Specific interactions of mycosubtilin with cholesterol-containing artificial membranes. Langmuir 27: 10785-10792.
Nihorimbere, V., Fickers, P., Thonart, P., and Ongena, M. (2009) Ecological fitness of Bacillus subtilis BGS3 regarding production of the surfactin lipopeptide in the rhizosphere. Environ Microbiol Rep 1: 124-130.
Nihorimbere, V., Cawoy, H., Seyer, A., Brunelle, A., Thonart, P., and Ongena, M. (2012) Impact of rhizosphere factors on cyclic lipopeptide signature from the plant beneficial strain Bacillus amyloliquefaciens S499. FEMS Microbiol Ecol 79: 176-191.
Niu, B., Rueckert, C., Blom, J., Wang, Q., and Borriss, R. (2011) The genome of the plant growth-promoting rhizobacterium Paenibacillus polymyxa M-1 contains nine sites dedicated to nonribosomal synthesis of lipopeptides and polyketides. J Bacteriol 193: 5862-5863.
Ongena, M., and Jacques, P. (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16: 115-125.
Ongena, M., Jacques, P., Touré, Y., Destain, J., Jabrane, A., and Thonart, P. (2005a) Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Appl Microbiol Biotechnol 69: 29-38.
Ongena, M., Duby, F., Jourdan, E., Beaudry, T., Jadin, V., Dommes, J., etal. (2005b) Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Appl Microbiol Biotechnol 67: 692-698.
Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., etal. (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9: 1084-1090.
Pérez-García, A., Romero, D., and de Vicente, A. (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of bacilli in agriculture. Curr Opin Biotechnol 22: 187-193.
Pertot, I., Puopolo, G., Hosni, T., Pedrotti, L., Jourdan, E., and Ongena, M. (2013) Limited impact of abiotic stress on surfactin production in planta and on disease resistance induced by Bacillus amyloliquefaciens S499 in tomato and bean. FEMS Microbiol Ecol 86: 505-519.
Raaijmakers, J.M., and Mazzola, M. (2012) Diversity and natural functions of antibiotics produced by beneficial and plant pathogenic bacteria. Annu Rev Phytopathol 50: 403-424.
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.
van Rij, E.T., Girard, G., Lugtenberg, B.J.J., and Bloemberg, G.V. (2005) Influence of fusaric acid on phenazine-1-carboxamide synthesis and gene expression of Pseudomonas chlororaphis strain PCL1391. Microbiology 151: 2805-2814.
Romero, D., De Vicente, A., Rakotoaly, R.H., Dufour, S.E., Veening, J.W., Arrebola, E., etal. (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.
Rückert, C., Blom, J., Chen, X., Reva, O., and Borriss, R. (2011) Genome sequence of B. amyloliquefaciens type strain DSM7T reveals differences to plant-associated B. amyloliquefaciens FZB42. J Biotechnol 155: 78-85.
Shen, L., Wang, F., Liu, Y., Qian, Y., Yang, J., and Sun, H. (2013) Suppression of tobacco mosaic virus by Bacillus amyloliquefaciens strain Ba33. J Phytopathol 161: 293-294.
Stein, T. (2005) Bacillus subtilis antibiotics: structures, synthesis and specifics functions. Mol Microbiol 56: 845-847.
Touré, Y., Ongena, M., Jacques, P., Guiro, A., and Thonart, P. (2004) Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J Appl Microbiol 96: 1151-1160.
Wong, W.C., and Preece, T.F. (1979) Identification of Pseudomonas tolaasi: the white line in agar and mushroom tissue block rapid pitting tests. J Appl Bacteriol 47: 401-407.
Wu, X.C., Shen, X.B., Ding, R., Qian, C.D., Fang, H.H., and Li, O. (2010) Isolation and partial characterization of antibiotics produced by Paenibacillus elgii B69. FEMS Microbiol Lett 310: 32-38.
Xu, H.M., Rong, Y.J., Zhao, M.X., Song, B., and Chi, Z.M. (2014) Antibacterial activity of the lipopetides produced by Bacillus amyloliquefaciens M1 against multidrug-resistant Vibrio spp. isolated from diseased marine animals. Appl Microbiol Biotechnol 98: 127-136.
Yang, P., Sun, Z.X., Liu, S.Y., Lu, H.X., Zhou, Y., and Sun, M. (2013) Combining antagonistic endophytic bacteria in different growth stages of cotton for control of Verticillium wilt. Crop Prot 47: 17-23.
Yuan, J., Raza, W., Huang, Q., and Shen, Q. (2012) The ultrasound-assisted extraction and identification of antifungal substances from B. amyloliquefaciens strain NJN-6 suppressing Fusarium oxysporum. J Basic Microbiol 52: 721-730.