Lipopeptide biodiversity in antifungal Bacillus strains isolated from Algeria
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Abstract
Several Bacillus strains have been well studied for their ability to control soil-borne plant diseases. This property is linked to the production of several families of lipopeptides. Depending of their structure, these compounds show antifungal and/or plant systemic resistance inducing activities. In this work, the biodiversity of lipopeptides produced by different antifungal Bacillus strains isolated from seeds, rhizospheric, and non-rhizospheric soils in Algeria was analyzed. Sixteen active strains were characterized by PCR for their content in genes involved in lipopeptide biosynthesis and by MALDI-ToF for their lipopeptide production, revealing a high biodiversity of products. The difficulty to detect kurstakin genes led us to design two new sets of specific primers. An interesting potential of antifungal activity and the synthesis of two forms of fengycins differing in the eighth amino acid (Gln/Glu) were found from the strain 8. Investigation of its genome led to the finding of an adenylation domain of the fengycin synthetase predicted to activate the glutamate residue instead of the glutamine one. According to the comparison of both the results of MALDI-ToF-MS and genome analysis, it was concluded that this adenylation domain could activate both residues at the same time. This study highlighted that the richness of the Algerian ecosystems in Bacillus strains is able to produce: surfactin, pumilacidin, lichenysin, kurstakin, and different types of fengycins.
Keywords
Lipopeptides Kurstakin Specific primers Fengycin Algerian Bacillus strainsNotes
Acknowledgements
This work has been carried out in the framework of Alibiotech project which is financed by European Union, French State, and the French Region of Hauts-de-France and of INTERREG Va SMARTBIOCONTROL portfolio (Bioscreen Project) which is financed by European Union and Walloon Region.
Supplementary material
References
- Abderrahmani A, Tapi A, Nateche F, Chollet M, Leclère V, Wathelet B, Hacene H, Jacques P (2011) Bioinformatics and molecular approaches to detect NRPS genes involved in the biosynthesis of kurstakin from Bacillus thuringiensis. Appl Microbiol Biotechnol 92:571–581CrossRefPubMedGoogle Scholar
- Asselbergh B, Curvers K, Franca S-C, Audenaert K, Vuylsteke M, Van Breusegem F, Höfte M (2007) Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol 144:1863–1877CrossRefPubMedPubMedCentralGoogle Scholar
- 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, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9Google Scholar
- Béchet M, Caradec T, Hussein W, Abderrahmani A, Chollet M, Leclère V, Dubois T, Lereclus D, Pupin M, Jacques P (2012) Structure, biosynthesis and properties of kurstakins, nonribosomal lipopeptides from Bacillus spp. Appl Microbiol Biotechnol 95:593–600CrossRefPubMedGoogle Scholar
- Biniarz P, Lucaszewicz M, Janek T (2017) Screening concepts, characterization and structural analysis of microbial-derived bioactive lipopeptides: a review. Crit Rev Biotechnol 37:393–410CrossRefPubMedGoogle Scholar
- Brettin T, Davis J-J, Disz T, Edwards R-A, Gerdes S, Olsen G-J, Olson R, Overbeek R, Parrello B, Pusch G-D, Shukla M, Thomason J-A, Stevens R, Vonstein V, Wattam A-R, Xia F (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365CrossRefPubMedPubMedCentralGoogle Scholar
- Christiansen G, Philmus B, Hemscheidt T, Kurmayer R (2011) Genetic variation of adenylation domains of the anabaenopeptin synthesis operon and evolution of substrate promiscuity. J Bacteriol 193:3822–3831CrossRefPubMedPubMedCentralGoogle Scholar
- Coutte F, Lecouturier D, Dimitrov K, Guez J-S, Delvigne F, Dhulster P, Jacques P (2017) Microbial lipopeptide production and purification bioprocesses, current progress and future challenges. Biotechnol J DOI. https://doi.org/10.1002/biot.201600566 CrossRefGoogle Scholar
- Crawford J-M, Portmann C, Kontnik R, Walsh C-T, Clardy J (2011) NRPS substrate promiscuity diversifies the xenematides. Org Lett 13:5144–5147CrossRefPubMedPubMedCentralGoogle Scholar
- Deravel J, Lemière S, Coutte F, Krier F, Van Hese N, Béchet M, Sourdeau N, Höfte M, Leprêtre A, Jacques P (2014) Mycosubtilin and surfactin are efficient, low ecotoxicity molecules for the biocontrol of lettuce downy mildew. Appl Microbiol Biotechnol 98:6255–6264CrossRefPubMedGoogle Scholar
- Esmaeel Q, Chevalier M, Chataigné G, Subashkumar R, Jacques P, Leclère V (2016) Nonribosomal peptide synthetase with a unique iterative-alternative-optional mechanism catalyzes amonabactin synthesis in Aeromonas. Appl Microbiol Biotechnol 100:8453–8463CrossRefPubMedGoogle Scholar
- Flissi A, Dufresne Y, Michalik J, Tonon L, Janot S, Noe L, Jacques P, Leclère V, Pupin M (2016) Norine, the knowledgebase dedicated to nonribosomal peptides, is now open to crowdsourcing. Nucleic Acids Res 44:D1113-D1118CrossRefGoogle Scholar
- Hathout Y, Ho Y-P, Ryzhov V, Demirev P, Fenselau C (2000) Kurstakins: a new class of lipopeptides isolated from Bacillus thuringiensis. J Nat Prod 63:1492–1496CrossRefPubMedGoogle Scholar
- Jacobs A (2007) Transport bactérien en milieux poreux: Expérimentations et Modélisation. Migration de bactéries issues de boues de STEP. Thèse de Doctorat. Université d’Avignon, FranceGoogle Scholar
- Jacques P (2011) Surfactin and other lipopeptides from Bacillus spp. In Biosurfactant Microbiology Monographs. Edited by Soberon-Chavez G, Springer-Verlag, Berlin Heidelberg 20: pp 57–91Google Scholar
- Jullien N (2012) AmplifX 1.7.0. Website http://crn2m.univ-mrs.fr/pub/amplifx-list
- Li X-Y, Mao Z-C, Wang Y-H, Wu Y-X, He Y-Q, Long C-L (2012) ESI LC-MS and MS/MS characterization of antifungal cyclic lipopeptides produced by Bacillus subtilis XF-1. J Mol Microbiol Biotechnol 22:83–93CrossRefPubMedGoogle Scholar
- Luo C, Liu X, Zhou H, Wang X, Chen Z (2015a) Nonribosomal peptide synthase gene clusters for lipopeptide biosynthesis in Bacillus subtilis 916 and their phenotypic functions. Appl Environ Microbiol 81:422–431CrossRefPubMedGoogle Scholar
- Luo C, Liu X, Zhou X, Guo J, Truong J, Wang X, Zhou H, Li X, Chen Z (2015b) Unusual biosynthesis and structure of locillomycins from Bacillus subtilis 916. Appl Environ Microbiol 81:6601–6609CrossRefPubMedPubMedCentralGoogle Scholar
- Marahiel M-A, Stachelhaus T, Mootz H-D (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev 97:2651–2674CrossRefPubMedGoogle Scholar
- Mootz H-D, Marahiel M-A (1997)) The tyrocidine biosynthesis operon of Bacillus brevis: complete nucleotide sequence and biochemical characterization of functional internal adenylation domains. J Bacteriol 179:6843–6850CrossRefPubMedPubMedCentralGoogle Scholar
- Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125CrossRefPubMedGoogle Scholar
- Overbeek R, Olson R, Pusch G-D, Olsen G-J, Davis J-J, Disz T, Edwards R-A, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam A-R, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42:D206-D214CrossRefGoogle Scholar
- Pathak K-V, Keharia H, Gupta K, Thakur S-S, Balaram P (2012) Lipopeptides from the banyan endophyte, Bacillus subtilis K1: mass spectrometric characterization of a library of fengycins. J Am Soc Mass Spectrom 23:1716–1728CrossRefPubMedGoogle Scholar
- Peypoux F, Guinand M, Michel G, Delcambe L, Das B-C, Lederer E (1978) Structure of iturin A, a peptidolipid antibiotic from Bacillus subtilis. Biochemistry 17:3992–3996CrossRefPubMedGoogle Scholar
- Raaijmakers J-M, Paulitz C-T, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: A playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361CrossRefGoogle Scholar
- Stachelhaus T-H, Mootz H-D, Marahiel M-A (1999) The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol 6:493–505CrossRefPubMedGoogle Scholar
- Tapi A, Chollet-Imbert M, Scherens B, Jacques P (2010) New approach for the detection of non ribosomal peptide synthetase genes in Bacillus strains by polymerase chain reaction. Appl Microbiol Biotechnol 85:1521–1531CrossRefPubMedGoogle Scholar
- Van Beneden S, Pannecoucque J, Debode J, De Backer G, Höfte M (2009) Characterisation of fungal pathogens causing basal rot of lettuce in Belgian greenhouses. Eur J Plant Pathol 124:9–19CrossRefGoogle Scholar
- Walker J-E, Abraham E-P (1970) The structure of bacilysin and other products of Bacillus subtilis. Biochem J 118:563–570CrossRefPubMedPubMedCentralGoogle Scholar
- Weber T, Blin K, Duddela S, Krug D, Kim H-U, Bruccoleri R, Lee S-Y, Fischbach M-A, Müller R, Wohlleben W, Breitling R, Takano E, Medema M-H (2015) antiSMASH 3.0 - a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237-W243CrossRefPubMedCentralGoogle Scholar
- Yamamoto S, Harayama S (1995) PCR amplification and direct sequencing of gyrB genes with universal primers and their application to the detection and taxonomic analysis of Pseudomonas putida strains. Appl Environ Microbiol 61:1104–1109PubMedPubMedCentralGoogle Scholar