Hyperdiverse, bioactive, and interaction-specific metabolites produced only in co-culture suggest diverse competitors may fuel secondary metabolism of xylarialean fungi
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Xylariales is one of the largest and most ecologically diverse fungal orders. Xylarialean fungi are well-known for their chemical diversity, reflecting a hyperdiversity of biosynthetic gene clusters (BCGs), even compared to other bioactive fungi. Enhanced secondary metabolism appears linked to the number of horizontal gene transfer (HGT) events and gene duplications, which is highest in the clade that also has a greater ability to both degrade lignocellulose as saprotrophs and interact with a wider variety of plant and lichen hosts as symbiotic endophytes. Thus, one hypothesis for BGC diversification in this clade is that diverse competitive interactions—in both their free-living and symbiotic life stages—may exert selective pressure for HGT and a diverse metabolic repertoire. Here, we tested this hypothesis using untargeted metabolomics to examine how pairwise co-culture interactions between seven xylarialean fungi influenced their metabolite production. Overall, we detected >9,000 features, including putatively anti-microbial, insecticidal, and medicinal compounds. In total, 6,115 features were over-represented in co- cultures vs. 2,071 in monocultures. No features occurred in all 21 interactions, and only 39% of features occurred in >10 different co-culture combinations. Each additional co-culture interaction resulted in an 11 to 14-fold increase in metabolite richness. Consistent with HGT, metabolite profiles did not reflect phylogenetic relationships. Overall, the diversity and specificity of metabolites support the role of widespread and diverse competitive interactions to drive diversification of xylarialean metabolism. Additionally, as plant hormones were only detected in co-culture, our results also reveal how competition may influence the outcome of endophytic symbioses.
Importance
Saprotrophic and endophytic xylarialean fungi are among the most prolific producers of bioactive secondary metabolites, which are often encoded by sets of physically clustered genes (i.e., biosynthetic gene clusters). Secondary metabolites have numerous industrial uses as antibiotics, pharmaceuticals, and insecticidal toxins, but their ecological importance for competitive and symbiotic interactions with other fungi, bacteria, and plants is not fully understood. Here, we examined how co-culture interactions with ecologically and genetically diverse competitors influence the metabolite production of seven xylarialean strains. Among 21 pairwise interactions, we detected >9,000 metabolite features, 67% of which were produced only in specific co-cultures and not in monocultures. Over 8,000 features were unclassified at any level and likely represent novel bioactive compounds. Our data illustrate that competitor identity and ecology significantly impact xylarialean fungal secondary metabolite production, key information that will enable us to further harness the immense biotechnological potential of these fungi.
