Multi-meta-omics reveal unique symbiotic synchronization between ectomycorrhizal fungus and soil microbiome in Tricholoma matsutake habitat.

BACKGROUND

Ectomycorrhizal (ECM) fungi establish symbiotic relationships with plant roots, enhancing nutrient uptake, improving plant health, and boosting ecosystem resilience. Although previous studies reported molecular interactions among plant-ECM fungi-surrounding microbes near plant roots, microbiome-wide metabolic shifts and associations with the fungi remain unclear.

RESULTS

Using Tricholoma matsutake as a model, we initially found that T. matsutake induced remarkable microbial community turnover linked to altered soil moisture, nitrogen, and phosphorus levels. Parallel with the compositional alteration, microbiome-wide metabolic capacities, including glutamate metabolism, oligopeptide transport, and siderophore activity, were enriched in the T. matsutake-colonizing soil compared to the soils where the fungus was not colonized. From metatranscriptome data, we found that T. matsutake induced functional remodeling in nitrogen metabolism. Notably, the fungus and soil microbiome were metabolically synchronized with the upregulation of nitrate reduction, glutamate biosynthesis, tryptophan biosynthesis, and indole-3-acetic acid (IAA) biosynthesis. Metabarcoding and metatranscriptome-guided microbial associations revealed potential T. matsutake helper bacteria consisting of Conexibacter and Paraburkholderia. Phage community analyses further showed that the colonization of the ECM fungus influenced phage distributions along with the increase in temperate phage populations. The differential expression of auxiliary metabolic genes also demonstrated that phages could influence bacterial fitness in response to T. matsutake colonization.

CONCLUSION

Our multi-meta-omics-based approaches revealed unique environmental changes by T. matsutake compared to other mycorrhizal systems, as well as metabolic synchronization between the ECM fungus and surrounding microbiomes. These findings will expand our understanding of ECM symbiotic frameworks by highlighting integrated microbial and viral metabolic dynamics. Video Abstract.