Abstract
ABSTRACTSmall-molecule signaling is one major mode of communication within the polymicrobial consortium of soil and rhizosphere. While microbial secondary metabolite (SM) production and responses of individual species have been studied extensively, little is known about potentially conserved roles of SM signals in multilayered symbiotic or antagonistic relationships. Here, we characterize the SM-mediated interaction between the plant-pathogenic bacterium Ralstonia solanacearum and the two plant-pathogenic fungi Fusarium fujikuroi and Botrytis cinerea. We show that cellular differentiation and SM biosynthesis in F. fujikuroi are induced by the bacterially produced lipopeptide ralsolamycin (synonym ralstonin A). In particular, fungal bikaverin production is induced and preferentially accumulates in fungal survival spores (chlamydospores) only when exposed to supernatants of ralsolamycin-producing strains of R. solanacearum. Although inactivation of bikaverin biosynthesis moderately increases chlamydospore invasion by R. solanacearum, we show that other metabolites such as beauvericin are also induced by ralsolamycin and contribute to suppression of R. solanacearum growth in vitro. Based on our findings that bikaverin antagonizes R. solanacearum and that ralsolamycin induces bikaverin biosynthesis in F. fujikuroi, we asked whether other bikaverin-producing fungi show similar responses to ralsolamycin. Examining a strain of B. cinerea that horizontally acquired the bikaverin gene cluster from Fusarium, we found that ralsolamycin induced bikaverin biosynthesis in this fungus. Our results suggest that conservation of microbial SM responses across distantly related fungi may arise from horizontal transfer of protective gene clusters that are activated by conserved regulatory cues, e.g., a bacterial lipopeptide, providing consistent fitness advantages in dynamic polymicrobial networks.
Highlights
Small-molecule signaling is one major mode of communication within the polymicrobial consortium of soil and rhizosphere
Using an in vitro coculture assay (Fig. 1A), we found that ralsolamycin induces pigment production in three Fusarium species: F. fujikuroi, F. graminearum, and F. oxysporum f. sp. lycopersici (Fig. S1A)
We did not observe any specific signals for fusarubin production (MW of 306 [Fig. S1B]), suggesting that the red pigmentation at the coculture interface was primarily due to bikaverin production
Summary
Small-molecule signaling is one major mode of communication within the polymicrobial consortium of soil and rhizosphere. Many soil microbes are equipped with an arsenal of unique biosynthetic enzymes, producing bioactive molecules that are thought to help them secure a niche in their local environment These compounds are often termed secondary metabolites (SMs) because they are seemingly dispensable in axenic culture, the genes involved in their production can account for large proportions of some microbial genomes and are evolutionarily maintained, suggesting that they are indispensable in a natural environment. The lipopeptide ralsolamycin (synonym ralstonin A), produced by a hybrid polyketide synthase/nonribosomal peptide synthetase (PKS-NRPS) biosynthetic gene cluster (rmy) [7, 9, 10], was shown to induce chlamydospore formation in a phylogenetically diverse panel of plant-associated and/or soil-inhabiting fungi representing members of the Mucoromycota, Ascomycota, and Basidiomycota [7].
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