Winter cover cropping increases synergistic species interactions and plant growth-promoting traits involved in phosphorus and nitrogen cycling in rice rhizosphere microbiome

Phosphorus (P) and nitrogen (N) cycling in paddy soils is essential for sustaining global rice production. However, mineral fertilization efficiency is limited by substantial N losses and strong soil-driven P fixation. This study explored the potential of winter cover crops incorporated before rice seeding to stimulate microorganisms involved in nutrient cycling. Microbial genomics and cultivation-based approaches were integrated to investigate bacterial, archaeal and fungal communities in the rhizosphere compartments (rhizosphere soil, rhizoplane, root endosphere) of rice cultivated with or without hairy vetch ( Vicia villosa ) as cover crop in a temperate European rice district. Microbial diversity and community composition were significantly shaped by plant species (rice, vetch) and compartments. Cover cropping increased the abundance of cultured and uncultured microorganisms able to solubilize and mineralize inorganic and organic P species, and of mycorrhizal fungi, with a corresponding increase of bioavailable P. Moreover, a higher number of bacterial strains with plant growth-promoting traits, including diazotrophy, production of indole acetic acid, extracellular polymeric substances and siderophores, was isolated from cover-cropped rice plants. Network analysis evidenced a 40 % increase in synergistic microbial interactions, with P-solubilizing/mineralizing genera like Cladosporium and Penicillium but also uncharacterized ammonia-oxidizing archaea playing a key role. Rhizoplane hosted a higher percentage of culturable strains with P- and N-cycling potential (>90 %), compared to other rhizosphere compartments (75 %), emerging as a crucial boundary among soil-plant-microbiome ecosystems. This work gives a microbial perspective to the benefits of winter cover cropping for improving nutrient pools in paddy soils, providing valuable insights to support sustainable agronomic practices.