Biodiversity of key-stone phylotypes determines crop production in a 4-decade fertilization experiment

Cropping systems have fertilized soils for decades with undetermined consequences for the productivity and functioning of terrestrial ecosystems. One of the critical unknowns is the role of soil biodiversity in controlling crop production after decades of fertilization. This knowledge gap limits our capacity to assess how changes in soil biodiversity could alter crop production and soil health in changing environments. Here, we used multitrophic ecological networks to investigate the importance of soil biodiversity, in particular, the biodiversity of key-stone taxa in controlling soil functioning and wheat production in a 35-year field fertilization experiment. We found strong and positive associations between soil functional genes, crop production and the biodiversity of key-stone phylotypes; soils supporting a larger number of key-stone nematode, bacteria and fungi phylotypes yielded the highest wheat production. These key-stone phylotypes were also positively associated with plant growth (phototrophic bacteria, nitrogen fixers) and multiple functional genes related to nutrient cycling. The retrieved information on the genomes clustered with key-stone bacterial phylotypes indicated that the key-stone taxa had higher gene copies of oxidoreductases (participating most biogeochemical cycles of ecosystems and linking to microbial energetics) and 71 essential functional genes associated with carbon, nitrogen, phosphorus, and sulfur cycling. Altogether, our work highlights the fundamental role of the biodiversity of key-stone phylotypes in maintaining soil functioning and crop production after several decades of fertilization, and provides a list of key-stone phylotypes linking to crop production and soil nutrient cycling, which could give science-based guidance for sustainable food production.