Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems

TLDR

Microorganisms are central to soil phosphorus cycling, yet their functional responses to long‑term nutrient inputs remain largely unknown. The study aimed to assess how long‑term nitrogen and phosphorus inputs alter the relative abundance of microbial P‑transformation genes. Metagenomic sequencing was performed at four experimental sites that had received varied N and P inputs for up to 39 years to quantify gene abundance changes. Long‑term P fertilization promoted microbial P immobilization by shifting gene abundances (decreasing phoR and increasing pit), whereas long‑term N fertilization lowered soil pH, reduced P‑solubilizing genes and key bacterial groups, and weakened gene linkages, challenging the view that P‑solubilization is governed by N:P stoichiometry and showing that N inputs diminish, while P inputs enhance, microbial P cycling functions.

Abstract

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.