Fairy ring fungi are ecosystem engineers accelerating nitrogen cycling to promote plant productivity in grasslands

Fairy rings are widespread features in grasslands worldwide, accompanied by lush dark-green vegetation bands. This enigmatic feature is caused by increased soil bioavailable nitrogen (N) due to the expansion of fairy ring fungi (FRF), mostly basidiomycetous fungi. However, little is known about how FRF enhance soil bioavailable N concentrations. Here, we conducted a survey of 35 fairy rings in temperate grasslands to reveal soil N cycling responses using amplicon and metagenomic sequencing. The presence of FRF accelerated organic N mineralization via promoting extracellular enzyme activity, leading to an 455% increase in ammonium-N. This further increased nitrification by favoring ammonia-oxidizing archaea. Denitrification and N fixation were not affected by FRF, thus not explaining the phenomenon. The enhanced bioavailable N strongly increased plant N content and productivity indicated by luxuriant vegetation. Our results suggest that FRF can act as ecosystem engineers shaping fairy rings by driving soil N cycling.