Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization

As a homologous gene encoding microbial alkaline phosphomonoesterase, the expression of phoD is critically controlled by P availability and thus contributes to the mineralization of soil organic P under P-depleted condition. However, its role in the regulation of soil P turnover is largely unknown due to the complex coupling of physiochemical and biological processes in the P cycle, especially in paddy field. We hypothesized that 1) P fertilization would decrease the abundance of phoD gene and change the composition of phoD-harboring microbial community and 2) the high abundance of phoD-harboring microorganisms in P-poor soil would stimulate the synthesis of alkaline phosphomonoesterase, thus mitigating P limitation via the mineralization of organic P. After 42 days of rice growth, the phoD abundance negatively correlated with soil P availability, and it was significantly higher in non-fertilized treatments than in P-fertilized treatments for both rhizosphere and bulk soils. A stronger competition among phoD-harboring microorganisms was detected in non-fertilized soil than in P-fertilized soil, with Bradyrhizobium, Methylobacterium, and Methylomonas being the dominant taxa in all samples. However, the high phoD gene abundance under P-poor condition was mainly due to the growth of rare operational taxonomic units (OTUs) affiliated to Actinobacteria and Cyanobacteria (relative abundance < 3%). Consistent with our hypothesis, the growth of phoD-harboring microorganisms stimulated the hydrolysis of organic P in non-fertilized soil. However, in the P-fertilized treatments, the increase in OTU abundance was accompanied by the depletion of exchangeable P and accumulation of microbial biomass P. Our findings suggest that phoD-harboring microorganisms have the potential to immobilize P in biomass when the supply is sufficient while mineralize organic P under P-poor condition, during which the rare taxa play an important role.