Bacillus subtilis, microbial ecology; Lipopeptides; gene expression, in vivo
Abstract :
[en] Cyclic lipopeptides and particularly surfactins produced
by Bacillus species retain antibacterial, antiviral,
biofilm-forming and plant resistance-inducing
activities. In most cases, their role in biological
control of plant diseases was evoked on the basis
of in vitro assays or by using non-producing/
overproducing mutants but there is a need for more
direct evidence of an efficient lipopeptide biosynthesis
in the rhizosphere. In this work, we coupled
LC-MS quantification of the lipopeptides secreted by
cells colonizing tomato plants with the use of psrfA–
lacZ reporter system integrated within the BGS3
chromosome to study the expression of the surfactin
operon in planta. Results showed that a higher
level of psrfA induction was observed upon the
establishment of a stable BGS3 population on roots
and surfactins extracted from the rhizosphere were
produced in biologically significant quantities. Our
results also demonstrate that BGS3 efficiently utilizes
the main substrates from plant exudates to
produce surfactins. This synthesis is also efficient
in cells forming colonies and the production may be
favoured in bacteria developing slowly in the rhizosphere.
This provides a first understanding of how
environmental factors may influence lipopeptide
production by beneficial Bacillus strains.
Asaka, O., and Shoda, M. (1996) Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl Environ Microbiol 62: 4081-4085.
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., Gilroy, S., and Vivanco, J.M. (2006) The role of root exudates in rhizosphere interations with plants and other organisms. Annu Rev Plant Biol 57: 233-266.
Dubern, J.F., and Bloemberg, G.V. (2006) Influence of environmental conditions on putisolvins I and II production in Pseudomonas putida strain PCL1445. FEMS Microbiol Lett 263: 169-175.
Duffy, B.K., and Défago, G. (1999) Environmental factors modulating antibiotic and siderophore biosynthesis by Pseudomonas fluorescens biocontrol strains. Appl Environ Microbiol 65: 2429-2438.
Eeman, M., Berquand, A., Dufrene, Y.F., Paquot, M., Dufour, S., and Deleu, M. (2006) Penetration of surfactin into phospholipid monolayers: nanoscale interfacial organization. Langmuir 22: 11337-11345.
Espinosa-Urgel, M., Kolter, R., and Ramos, J.L. (2002) Root colonization by Pseudomonas putida: love at first sight. Microbiol UK 148: 1-3.
Fickers, P., Leclère, V., Guez, J., Bechet, M., Coucheney, F., Joris, B., and Jacques, P. (2008) Temperature dependence of mycosubtilin homologue production in Bacillus subtilis ATCC6633. Res Microbiol 159: 449-457.
Guérout-fleury, A., Frandsen, N., and Stragier, P. (1996) Plasmid for ectopic integration in Bacillus subtillis. Gene 180: 57-61.
Guez, J.S., Muller, C.H., Danze, P.M., Buchs, J., and Jacques, P. (2008) Respiration activity monitoring system (RAMOS), an efficient tool to study the influence of the oxygen transfer rate on the synthesis of lipopeptide by Bacillus subtilis ATCC6633. J Biotechnol 134: 121-126.
Hirsch, A.M., Bauer, W.D., Bird, D.M., Cullimore, J., Tyler, B., and Yoder, J.I. (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84: 858-868.
Hojberg, O., Schnider, U., Winteler, H.V., Sorensen, J., and Haas, D. (1999) Oxygen-sensing reporter strain of Pseudomonas fluorescens for monitoring the distribution of low-oxygen habitats in soil. Appl Environ Microbiol 65: 4085-4093.
Jourdan, E., Henry, G., Duby, F., Dommes, J., Barthélemy, J.P., Thonart, P., and Ongena, M. (2009) Insights into the defense-related events occurring in plant cells following perceptions of surfactin-type lipopeptide from Bacillus subtilis. Mol Plant Microbe Interact (in press).
Kamilova, F., Kravchenko, L.V., Shaposhnikov, A.I., Makarova, N., and Lugtenberg, B. (2006) Effects of the tomato pathogen Fusarium oxysporum f. sp. radicislycopersici and of the biocontrol bacterium Pseudomonas fluorescens WCS365 on the composition of organic acids and sugars in tomato root exudate. Mol Plant Microbe Interact 19: 1121-1126.
Kim, P.I., Bai, H., Bai, D., Chae, H., Chung, S., Kim, Y., et al. (2004) Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J Appl Microbiol 97: 942-949.
Koumoutsi, A., Chen, X.H., Henne, A., Liesegang, H., Hitzeroth, G., Franke, P., et al. (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.
Kracht, M., Rokos, H., Ozel, M., Kowall, M., Pauli, G., and Vater, J. (1999) Antiviral and hemolytic activities of surfactin isoforms and their methyl ester derivatives. J Antibiot (Tokyo) 52: 613-619.
Lin, S.C., Lin, K.G., Lo, C.C., and Lin, Y.M. (1998) Enhanced biosurfactant production by a Bacillus licheniformis mutant. Enzyme Microb Technol 23: 267-273.
Lugtenberg, B.J.J., Dekkers, L., and Bloemberg, G.V. (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39: 461-490.
Mukherjee, S., Dasa, P., and Sen, R. (2006) Towards commercial production of microbial surfactants. Trends Biotechnol 24: 509-515.
Mulligan, C.N. (2005) Environmental applications for biosurfactants. Environ Pollut 133: 183-198.
Ongena, M., and Jacques, P. (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16: 115-125.
Ongena, M., Adam, A., Jourdan, E., Paquot, M., Brans, A., Joris, B., et al. (2007) Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ Microbiol 9: 1084-1090.
Ongena, M., Jourdan, E., Adam, A., Schaefer, M., Budzikiewicz, H., and Thonart, P. (2008) Amino acids, iron, and growth rate as key factors influencing production of the Pseudomonas putida BTP1 benzylamine derivative involved in systemic resistance induction in different plants. Microb Ecol 55: 280-292.
Peypoux, F., Bonmatin, J.M., and Wallach, J. (1999) Recent trends in the biochemistry of surfactin. Appl Microbiol Biotechnol 51: 553-563.
Rainey, P.B. (1999) Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol 1: 243-257.
Ramey, B.E., Koutsoudis, M., von Bodman, S.B., and Fuqua, C. (2004) Biofilm formation in plant-microbe associations. Curr Opin Microbiol 7: 602-609.
Romero, D., de Vicente, A., Rakotoaly, R.H., Dufour, S.E., Veening, J.W., Arrebola, E., et al. (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.
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.
Van Rij, E.T., Wesselink, M., Chin-A-Woeng, T.F.C., Bloemberg, G.V., and Lugtenberg, B.J.J. (2004) Influence of environmental conditions on the production of phenazine-1-carboxamide by Pseudomonas chlororaphis PCL1391. Mol Plant Microbe Interact 17: 557-566.
