Cereals rhizosphere microbiome undergoes host selection of nitrogen cycle guilds correlated to crop productivity

Sustainable transformation of agricultural plant production requires the reduction of nitrogen (N) fertilizer application. Such a reduced N fertilizer application may impede crop production due to an altered symbiosis of crops and their rhizosphere microbiome, since reduced N input may affect the competition and synergisms with the plant. The assessment of such changes in the crop microbiome functionalities at spatial scales relevant for agricultural management remains challenging. We investigated in a field plot experiment how and if the N cycling guilds of the rhizosphere of globally relevant cereal crops - winter barley, wheat and rye - are influenced by reduced N fertilization. Crop productivity was assessed by remote sensing of the shoot biomass. Microbial N cycling guilds were investigated by metagenomics targeting diazotrophs, nitrifiers, denitrifiers and the dissimilatory nitrate to ammonium reducing guild (DNRA). The functional composition of microbial N cycling guilds was explained by crop productivity parameters and soil pH, and diverged substantially between the crop species. The responses of individual microbial N cycling guild abundances to shoot dry weight and rhizosphere nitrate content was modulated by the N fertilization treatments and the crop species, which was identified based on regression analyses. Thus, characteristic shifts in the microbial N cycling guild acquisition associated with the crop host species were resolved. Particularly, the rhizosphere of rye was enriched with potentially N-preserving microbial guilds - diazotrophs and the DNRA guild - when no fertilizer was applied. We speculate that the acquisition of microbial N cycling guilds was the result of plant species-specific acquisition strategies. Thus, the investigated cereal crop holobionts have likely different symbiotic strategies that make them differently resilient against reduced N fertilizer inputs. Furthermore, we demonstrated that these belowground patterns of N cycling guilds from the rhizosphere microbiome are linked to remotely sensed aboveground plant productivity.