Harnessing the Mycosphere: Metagenomic Profiling of Mushroom Microbiomes and Spent Substrates for Plant Disease Suppression

Abstract

Soil-borne phytopathogens, including Fusarium oxysporum, Rhizoctonia solani, and Sclerotinia sclerotiorum, cause 20–40% annual global crop yield losses, necessitating sustainable alternatives to synthetic fungicides that have driven environmental degradation and resistance emergence. This review synthesizes current knowledge on metagenomic profiling of mushroom-associated microbiomes and spent mushroom substrate (SMS) as biological tools for pathogen suppression. Mushroom-forming fungi create distinct ecological niches the mycosphere and hyphosphere that selectively enrich antagonistic bacterial taxa including Bacillus, Pseudomonas, and Streptomyces through carbon exudate-mediated recruitment. Advanced shotgun metagenomic sequencing, coupled with bioinformatic platforms including antiSMASH for biosynthetic gene cluster identification and CAZy for carbohydrate-active enzyme annotation, has revolutionized our understanding of these suppressive communities. SMS, a globally abundant agricultural byproduct generating 4–5 kg per kilogram of harvested mushrooms, functions through multiple mechanisms: physical adsorption of phytotoxins such as fusaric acid, chemical antimicrobial compound release, and stimulation of copiotrophic microbial communities that intensify nutrient competition against pathogens. Synthetic microbial consortia (SynComs), rationally designed from mushroom-associated microbiomes, offer functional redundancy and ecological stability superior to single-strain biocontrol agents. Despite promising laboratory and greenhouse results, field translation faces challenges including ecological competence, soil heterogeneity, and raw SMS stabilization requirements. This review provides a comprehensive framework integrating metagenomic technologies, ecological principles, and practical applications for harnessing mushroom microbiomes in sustainable agriculture.