Metagenomic profiling reveals that divergent fire-adaptive strategies drive distinct fungal succession in pine litter decomposition.

Decomposing litter is a critical driver of fuel bed formation and forest fire regimes, yet how divergent plant fire-adaptive strategies influence litter chemistry and subsequent fungal decomposition dynamics remains poorly understood. Here, we conducted a 6-month reciprocal litterbag experiment by incubating litter from two contrasting pine species-the fire-tolerant Pinus taiwanensis and the fire-avoiding P. morrisonicola-in both their own native habitat and that of the other species, coupled with genome-resolved metagenomics to track fungal succession and lignocellulolytic functional profiles. We found that the fire-avoiding P. morrisonicola exhibited significantly accelerated decomposition, driven by inherently lower initial C:N ratio and less recalcitrant litter, whereas the fire-tolerant P. taiwanensis exhibited slower decomposition rates. Metagenomic profiling revealed a distinct functional succession underlying this process. Early decomposition was dominated by Ascomycota (e.g., Leotiomycetes), which rapidly colonized the litter to initiate biopolymer breakdown. As easily decomposable substrates depleted, a functional shift occurred. Specifically, the highly recalcitrant P. taiwanensis litter selectively recruited Basidiomycota (e.g., Agaricales and Trechisporales) equipped with diverse lignin-modifying enzymes, reflected by a late-stage temporal surge in ligninolytic gene abundances. Ultimately, these findings demonstrate that plant fire-adaptive strategies act as a strong filter, shaping litter chemistry to drive specific taxonomic and functional fungal succession. This study provides a mechanistic understanding of the eco-evolutionary linkage between plant traits, microbiome assembly, and ecosystem-level fire dynamics.