Mechanisms and impacts of Agaricus urinascens fairy rings on plant diversity and microbial communities in a montane Mediterranean grassland.

Abstract

Fungal fairy rings (FFRs) significantly influence plant communities and soil microbiota. This study investigated the development of Agaricus urinascens fairy rings in a species-rich montane Mediterranean grassland. By combining vegetation analysis, soil chemistry measurements, and next-generation sequencing, we assessed fairy rings' impact on soil properties, plants, fungi, and bacteria. Our findings reveal a fungal-driven transformation of biological communities, with significant variations across FFRs zones. At the fungal front (FF), plant biomass decreased slightly but increased more than threefold inside the ring (>1100 g/m²), favouring grasses like Brachypodium genuense over forbs. In addition, species richness dropped significantly in the FF (-40%) compared to surrounding grassland, particularly affecting perennials. Moreover, our findings reveal substantial alterations in soil properties at the FF, including a 534% increase in P₂O5, a 210% rise in electrical conductivity, and a 36% increase in soil hydrophobicity compared to the surrounding grassland. Clay content at the FF was nearly three times higher than outside the ring (162.8 vs. 57.5 g kg⁻¹), indicating potential structural modifications in the soil matrix. Organic carbon decreased by 10% in the FF, while the C/N ratio and cation exchange capacity dropped significantly. Distinct shifts in microbial composition were observed. Bacterial diversity declined at the FF, where Actinobacteria dominated (85%) and Proteobacteria dropped to 8%. Similarly, fungal diversity was lowest inside the ring but highest in the belt section, with Ascomycota reaching 97% at the FF. Certain taxa, such as Kribbella, Streptomyces, Trichoderma, Penicillium, and Dichotomopilus, coexisted with A. urinascens mycelium. Notably, hydrophobicity at the FF was linked to high calcium oxalate crystal coverage on fungal mycelium and plant roots. This may have accelerated root desiccation, ultimately leading to plant mortality. Overall, our findings provide strong evidence that fairy ring fungi act as ecosystem engineers, shaping the spatial patterns of biotic composition and diversity in Mediterranean grasslands.