Microorganisms play an important role in soil phosphorus (P) cycling and regulation of P availability in agroecosystems. However, the responses of the functional and ecological traits of P-transformation microorganisms to long-term nutrient inputs are largely unknown. This study used metagenomics to investigate changes in the relative abundance of microbial P-transformation genes at four long-term experimental sites that received various inputs of N and P nutrients (up to 39 years). Long-term P input increased microbial P immobilization by decreasing the relative abundance of the P-starvation response gene (phoR) and increasing that of the low-affinity inorganic phosphate transporter gene (pit). This contrasts with previous findings that low-P conditions facilitate P immobilization in culturable microorganisms in short-term studies. In comparison, long-term nitrogen (N) input significantly decreased soil pH, and consequently decreased the relative abundances of total microbial P-solubilizing genes and the abundances of Actinobacteria, Gammaproteobacteria, and Alphaproteobacteria containing genes coding for alkaline phosphatase, and weakened the connection of relevant key genes. This challenges the concept that microbial P-solubilization capacity is mainly regulated by N:P stoichiometry. It is concluded that long-term N inputs decreased microbial P-solubilizing and mineralizing capacity while P inputs favored microbial immobilization via altering the microbial functional profiles, providing a novel insight into the regulation of P cycling in sustainable agroecosystems from a microbial perspective.

Understanding the contribution of soil microbial communities to ecosystem processes is critical for predicting terrestrial ecosystem feedbacks under changing climate. Our current understanding lacks a consistent strategy to formulate the linkage between microbial systems and ecosystem processes due to the presumption of functional redundancy in soil microbes. Here we present a global soil microbial metagenomic analysis to generalize patterns of microbial taxonomic compositions and functional potentials across climate and geochemical gradient. Our analyses show that soil microbial taxonomic composition varies widely in response to climate and soil physicochemical gradients, while microbial functional attributes based on metagenomic gene abundances are redundant. Among 17 climate zones, microbial taxonomic compositions were more distinct than functional potentials, as climate and edaphic properties showed more significant influence on microbial taxonomic compositions than on functional potentials. Microbial taxonomies formed a larger and more complex co-occurrence network with more module structures than functional potentials. Functional network was strongly inter-connected among different categories, whereas taxonomic network was more positively interactive in the same taxonomic groups. This study provides strong evidence to support the hypothesis of functional redundancy in soil microbes, as microbial taxonomic compositions vary to a larger extent than functional potentials based on metagenomic gene abundances in terrestrial ecosystems across the globe.