Functional shifts in soil fungal communities regulate differential tree species establishment during subalpine forest succession

Soil fungi can differentially affect plant performance and community dynamics. While fungi play key roles in driving the plant-soil feedbacks (PSFs) that promote grassland succession, it remains unclear how the fungi-mediated PSFs affect tree species establishment during forest succession. We inoculated pioneer broadleaf (Betula platyphylla and Betula albosinensis) and nonpioneer coniferous tree seedlings (Picea asperata and Abies faxoniana) with fungal-dominated rooting zone soils collected from dominant plant species of early-, mid- and late-successional stages in a subalpine forest, and compared their biomass and fungal communities. All tree species accumulated abundant pathogenic fungi in early-successional inoculated soil, which generated negative biotic feedbacks and lowered seedling biomass. High levels of soil ectomycorrhizal fungi from mid- and late-successional stages resulted in positive biotic PSFs and strongly facilitated slow-growing coniferous seedling performance to favour successional development. B. albosinensis also grew better in mid- and late-successional soils with fewer pathogenic fungi than in early-successional soil, indicating its large susceptibility to pathogen attack. In contrast, the growth of another pioneer tree, B. platyphylla, was significantly suppressed in late-successional soil and was mostly driven by saprotrophic fungi, despite the unchanged pathogenic fungal community traits between the two fast-growing species. This unexpected result suggested a host specificity-dependent mechanism involved in the different impacts of fungal pathogens on host trees. Our findings reveal a critical role of functional shifts in soil fungal communities in mediating differential PSFs of tree species across successional stages, which should be considered to improve the prediction and management of community development following forest disturbances.