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BackgroundN fixation is one of the most important microbially driven ecosystem processes on Earth, allowing N to enter the soil from the atmosphere, and regulating plant productivity. A question that remains to be answered is whether such a fundamental process would still be that important in an over-fertilized world, as the long-term effects of fertilization on N fixation and associated diazotrophic communities remain to be tested. Here, we used a 35-year fertilization experiment, and investigated the changes in N fixation rates and the diazotrophic community in response to long-term inorganic and organic fertilization.ResultsIt was found that N fixation was drastically reduced (dropped by 50%) after almost four decades of fertilization. Our results further indicated that functionality losses were associated with reductions in the relative abundance of keystone and phylogenetically clustered N fixers such as Geobacter spp.ConclusionsOur work suggests that long-term fertilization might have selected against N fixation and specific groups of N fixers. Our study provides solid evidence that N fixation and certain groups of diazotrophic taxa will be largely suppressed in a more and more fertilized world, with implications for soil biodiversity and ecosystem functions.

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.

Organic matter application is a widely used practice to increase soil carbon content and maintain soil fertility. However, little is known about the effect of different types of organic matter, or the input of exogenous species from these materials, on soil fungal communities. In this study, fungal community composition was characterized from soils amended with three types of organic matter over a 30-year fertilization experiment. Chemical fertilization significantly changed soil fungal community composition and structure, which was exacerbated by the addition of organic matter, with the direction of change influenced by the type of organic matter used. The addition of organic matter significantly increased soil fungal richness, with the greatest richness achieved in soils amended with pig manure. Importantly, following addition of cow and pig manure, fungal taxa associated with these materials could be found in the soil, suggesting that these exogenous species can augment soil fungal composition. Moreover, the addition of organic matter decreased the relative abundance of potential pathogenic fungi. Overall, these results indicate that organic matter addition influences the composition and structure of soil fungal communities in predictable ways.

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