Tree traits drive phylogenetic and functional responses of soil fungal communities in Mediterranean forests subjected to recurrent fires

Abstract Wildfires are a natural disturbance in Mediterranean ecosystems, where plant species have usually developed fire-adaptive traits. In these fire-dependent ecosystems, fire-resistant fungal communities might co-evolve with fire-adapted plant communities, and long-term ecosystem stability may be a matter, not only of plants but also of associated soil fungi, particularly mycorrhizal species. In this study, we investigated the soil fungal phylogenetic diversity and structure (ITS1-MiSeq, Net Relatedness, and phylogenetic structure indices) and functioning (soil enzymatic activities) in Mediterranean Pinus halepensis Mill. forests from two zones with contrasting fire regimes. We further aimed to differentiate the effects of tree genotypes (single nucleotide polymorphism assay for Pinus spp. fire-adaptive candidate genes) and phenotypes from those of environmental factors such as climate and soil conditions on fungal phylogenetic assembly and community. Under high fire recurrence regime, the phylogenetic diversity of soil fungal communities decreased. Their phylogenetic structure also changed with fire regime, and pointed to a clustered community within the Basidiomycota clade. Fungal phylogenetic indices and higher abundances of ectomycorrhizal fungi under high fire recurrence were significantly related to higher activities of soil enzymes involved in nitrogen and phosphorus mobilization. The phylogenetic diversity and structure of soil fungal communities was primarily regulated by the phenotype of trees, and to a lesser extent by their genotype, while neither local climatic and soil conditions appeared to play a role. Our results suggest that long-term fire-induced changes in plant community occur with changes in phylogenetic and compositional shifts in soil fungal community with potential consequences for nutrient cycling. We propose that the adaptation of P. halepensis to recurrent fires may partly depend on the association with soil symbiotic fungi.