Statistical inference of keystone taxa reshaping the assembly rules of forest root microbiomes

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Abstract

Root-associated fungi and bacteria play pivotal roles in plant nutrient acquisition and stress tolerance. However, identifying the keystone taxa that have the greatest impacts on below-ground microbial assembly remains a major challenge. Here, we present a statistical framework for identifying microbes that could govern the assembly rules of complex plant microbiomes. Using more than 1,000 root samples collected from a cool-temperate forest, we reconstructed the architecture of “assembly landscapes” that depict the probability distributions of community states. We found that several endophytic fungi ( Oidiodendron , Cladophialophora , Hyaloscypha , and Meliniomyces ) could reorganize assembly landscape topography, potentially driving drastic shifts in mycorrhizal symbiotic types in host plants associated with both ectomycorrhizal and arbuscular mycorrhizal fungi ( Populus , Acer , and Juglans ). Furthermore, cross-kingdom effects of uncharacterized bacteria (e.g., Thermosporothrix ) on fungal community assembly were detected. We also found that prokaryotic communities underwent transitions among states characterized respectively by core (common) members, Pseudomonadota, and Actinomycetota under the disproportionate influence of " Candidatus Udaeobacter " and several endophytic fungi. Thus, data-driven inference of assembly landscapes will advance our understanding of underappreciated drivers of ecosystem-scale processes.

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