Abstract
Orfamide-type cyclic lipopeptides (CLPs) are biosurfactants produced by Pseudomonas and involved in lysis of oomycete zoospores, biocontrol of Rhizoctonia and insecticidal activity against aphids. In this study, we compared the biosynthesis, structural diversity, in vitro and in planta activities of orfamides produced by rhizosphere-derived Pseudomonas protegens and related Pseudomonas species. Genetic characterization together with chemical identification revealed that the main orfamide compound produced by the P. protegens group is orfamide A, while the related strains Pseudomonas sp. CMR5c and CMR12a produce orfamide B. Comparison of orfamide fingerprints led to the discovery of two new orfamide homologs (orfamide F and orfamide G) in Pseudomonas sp. CMR5c. The structures of these two CLPs were determined by nuclear magnetic resonance (NMR) and mass spectrometry (MS) analysis. Mutagenesis and complementation showed that orfamides determine the swarming motility of parental Pseudomonas sp. strain CMR5c and their production was regulated by luxR type regulators. Orfamide A and orfamide B differ only in the identity of a single amino acid, while orfamide B and orfamide G share the same amino acid sequence but differ in length of the fatty acid part. The biological activities of orfamide A, orfamide B, and orfamide G were compared in further bioassays. The three compounds were equally active against Magnaporthe oryzae on rice, against Rhizoctonia solani AG 4-HGI in in vitro assays, and caused zoospore lysis of Phytophthora and Pythium. Furthermore, we could show that orfamides decrease blast severity in rice plants by blocking appressorium formation in M. oryzae. Taken all together, our study shows that orfamides produced by P. protegens and related species have potential in biological control of a broad spectrum of fungal plant pathogens.
Highlights
The majority of natural rhizosphere soil microorganisms in various ecosystems is composed of Proteobacteria (Philippot et al, 2013)
Orfamide synthases contain three non-ribosomal peptide synthases (NRPSs) structural genes designed as ofaA, ofaB, and ofaC, which respectively encode two, four, and four amino acids (Figure 1)
Orfamide-synthases of these Pseudomonas strains contain two terminal thioesterase (TE) domains, which cleave the peptides from the NRPSs (Figure 1)
Summary
The majority of natural rhizosphere soil microorganisms in various ecosystems is composed of Proteobacteria (Philippot et al, 2013) Within this group rhizosphere-derived fluorescent pseudomonads have received a lot of attention as biocontrol agents in the past few decades (Höfte and Altier, 2010; Olorunleke et al, 2015a). Pseudomonas species show an enormous metabolic versatility and some isolates produce a remarkable spectrum of secondary metabolites both in vitro and in vivo conditions These secondary metabolites are indispensably involved in interspecies interactions in the soil environment (Raaijmakers and Mazzola, 2012). CLPs are amphiphilic molecules composed of a cyclic oligopeptide lactone ring coupled to a fatty acid tail (Raaijmakers et al, 2006, 2010). Pseudomonas derived CLPs are currently divided in eight different structural groups that differ in length and composition of the oligopeptide and fatty acid tail (Olorunleke et al, 2015a)
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