Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi

Abstract

Small-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.

Growing a circular economy with fungal biotechnology: a white paper

“…The SMs are synthesised by accessory biosynthetic pathways thought to be important for a range of processes, including spore development, spore survival and fungal communication. Recent advances promote the view that fungal mycotoxins are fitness factors that help to establish a niche for protection from competing microbes [101,102].…”

Bacteria‐induced production of the antibacterial sesquiterpene lagopodin B inCoprinopsis cinerea

“…The genomes of filamentous fungi are rich in gene clusters coding for biosynthetic pathways of SMs with various bioactivities, yet only few of them are expressed under laboratory conditions (Brakhage and Schroeckh, ; Chiang et al , ). The production of some SMs is induced in co‐cultures of fungi with bacteria (Cueto et al , ; Oh et al , ; Schroeckh et al , ; Ola et al , ; Spraker et al , ) and it has been hypothesized that these SMs function, depending on their concentration, either as signaling molecules or as growth inhibitors in the chemical defense of these fungi against bacterial competitors and antagonists (Brakhage et al , ; Andersson and Hughes, ; Netzker et al , ). Besides biotic stress, abiotic stress can also trigger expression of silent SM gene clusters (Scherlach and Hertweck, ; Gressler et al , ).…”

“…Besides biotic stress, abiotic stress can also trigger expression of silent SM gene clusters (Scherlach and Hertweck, ; Gressler et al , ). However, there are only few cases where the regulation of SM gene clusters involved in bacterial‐fungal interactions (BFIs) was studied at a molecular level (Schroeckh et al , ; Nützmann et al , ; Spraker et al , ). The SM gene clusters of filamentous fungi include non‐ribosomal peptide synthetases (NRPSs), polyketide synthases (PKSs) and terpene synthases (TSs) (Lackner et al , ; Bills et al , ).…”

Inhibition Mechanism of Caffeine in Tea Pathogenic Fungi Botryosphaeria Dothidea and Colletotrichum Gloeosporioides

“…And the melanin biosynthesis is an ideal target for development of targeted speci c inhibitor to control the fungal pathogens [39]. Schumacher [40] and Spraker et al [41] reported that the production of pigments in lamentous fungi was not directly involved in their growth and development, but that it might contribute to survival in unfavorable environmental stress conditions such as UV radiation, heat, and oxidation, bacterial invasion and pathogenesis related mechanisms. Based on this result, we hypothesize that melanin pigment might be the reason for the caffeine tolerance of the fungus.…”