Deciphering plant-beneficial fungal interactions: Unravelling metabolic diversity that underpins communication between Laccaria bicolor and Trichoderma

With over 250 known species, the genus Trichoderma (Ascomycota, Hypocreaceae) is found in various soils, on plant surfaces and as plant endophytes. While Trichoderma species are known as mycoparasites, their antagonistic behaviour can also negatively affect other beneficial fungi, such as mycorrhizal fungi. To gain insight into the metabolic signals involved in the interactions between the ectomycorrhizal fungus (ECM) Laccaria bicolor (Basidomycota, Hydnangiaceae), and different mycoparasitic Trichoderma spp. (T. harzianum strains WM24a1, MS8a1 and ES8g1, and T. atrobrunneum), we performed in vitro dual-confrontation experiments. We studied the volatile organic compounds (VOCs), hyphal metabolomes and soluble metabolites released by each of the fungi in various co-cultivation scenarios. The results revealed an altered growth of the mycelia depending on the degree of contact: When Trichoderma spp. and L. bicolor shared only the same headspace, Trichoderma spp. growth was at least partially inhibited, whereas in direct contact the growth of L. bicolor was impaired. Distinct strain- and species-specific changes in hyphal metabolites, in exudates and volatile emission were revealed from each of the studied fungi. We identified both core metabolite profiles and interaction-specific metabolic responses that were related to carbohydrate, lipid, nucleotide, energy and amino acid metabolisms. Volatile and soluble metabolites revealed temporal and spatial adjustments in dual cultures compared to solitary cultures, suggesting rapid contact-dependent adaptations and demonstrating the dynamic communication mechanisms between Trichoderma spp. and the ECM. These results suggest a central role for both emitted and secreted fungal metabolites in the fungal non-self-recognition and in interaction with each other.