Mycorrhizal and endophytic fungi structure forest below-ground symbiosis through contrasting but interdependent assembly processes.

Background: Interactions between plants and diverse root-associated fungi are essential drivers of forest ecosystem dynamics. The symbiosis is potentially dependent on multiple ecological factors/processes such as host/symbiont specificity, background soil microbiome, inter-root dispersal of symbionts, and fungus-fungus interactions within roots. Nonetheless, it has remained a major challenge to reveal the mechanisms by which those multiple factors/processes determine the assembly of root-associated fungal communities. Based on the framework of joint species distribution modeling, we examined 1,615 root-tips samples collected in a cool-temperate forest to reveal how root-associated fungal community structure was collectively formed through filtering by host plants, associations with background soil fungi, spatial autocorrelation, and symbiont-symbiont interactions. In addition, to detect fungi that drive the assembly of the entire root-associated fungal community, we inferred networks of direct fungus-fungus associations by a statistical modeling that could account for implicit environmental effects.

Results: The fine-scale community structure of root-associated fungi were best explained by the statistical model including the four ecological factors/processes. Meanwhile, among partial models, those including background soil fungal community structure and within-root fungus-fungus interactions showed the highest performance. When fine-root distributions were examined, ectomycorrhizal fungi tended to show stronger associations with background soil community structure and spatially autocorrelated patterns than other fungal guilds. In contrast, the distributions of root-endophytic fungi were inferred to depend greatly on fungus-fungus interactions. An additional statistical analysis further suggested that some endophytic fungi, such as Phialocephala and Leptodontidium, were placed at the core positions within the web of direct associations with other root-associated fungi.

Conclusion: By applying emerging statistical frameworks to intensive datasets of root-associated fungal communities, we demonstrated background soil fungal community structure and fungus-fungus associations within roots, as well as filtering by host plants and spatial autocorrelation in ecological processes, could collectively drive the assembly of root-associated fungi. We also found that basic assembly rules could differ between mycorrhizal and endophytic fungi, both of which were major components of forest ecosystems. Consequently, knowledge of how multiple ecological factors/processes differentially drive the assembly of multiple fungal guilds is indispensable for comprehensively understanding the mechanisms by which terrestrial ecosystem dynamics are organized by plant-fungal symbiosis.