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Microbes associated with phosphorus (P) cycling are intrinsic to soil P transformation and availability for plant use but are also influenced by the application of P fertilizer. Nevertheless, the variability in soil P in the field means that integrative analyses of soil P cycling, microbial composition, and microbial functional genes related to P cycling remain very challenging. In the present study in the North China Plain, we subjected the bacterial and fungal communities to amplicon sequencing analysis and characterized the alkaline phosphatase gene (phoD) encoding bacterial alkaline phosphatase in a long-term field experiment (10 years) with six mineral P fertilization rates up to 200 kg P ha–1. Long-term P fertilization increased soil available P, inorganic P, and total P, while soil organic P increased until the applied P rate reached 25 kg ha–1 and then decreased. The fungal alpha-diversity decreased as P rate increased, while there were no significant effects on bacterial alpha-diversity. Community compositions of bacteria and fungi were significantly affected by P rates at order and family levels. The number of keystone taxa decreased from 10 to 3 OTUs under increasing P rates from 0 to 200 kg ha–1. The gene copy numbers of the biomarker of the alkaline phosphatase phoD was higher at moderate P rates (25 and 50 kg ha–1) than at low (0 and 12.5 kg ha–1) and high (100 and 200 kg ha–1) rates of P fertilization, and was positively correlated with soil organic P concentration. One of the keystone taxa named BacOTU3771 belonging to Xanthomonadales was positively correlated with potential functional genes encoding enzymes such as glycerophosphoryl diester phosphodiesterase, acid phosphatase and negatively correlated with guinoprotein glucose dehydrogenase. Altogether, the results show the systematic effect of P gradient fertilization on P forms, the microbial community structure, keystone taxa, and functional genes associated with P cycling and highlight the potential of moderate rates of P fertilization to maintain microbial community composition, specific taxa, and levels of functional genes to achieve and sustain soil health.

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IntroductionA better understanding of the regulatory role of microorganisms on soil phosphorous (P) mobilization is critical for developing sustainable fertilization practices and reducing P resource scarcity. The phoD genes regulate soil organic P (Po) mobilization.MethodsBased on the long-term P application experiments in acid purple soil of maize system in Southwest China (started in 2010), the experiment included five P levels: 0, 16, 33, 49, and 65.5 kg P hm–2 (P0, P16, P33, P49, and P65.5, respectively). The molecular speciation of organic P in soil was determined by 31P-nuclear magnetic resonance (NMR), high-throughput sequencing technology, and real-time qPCR were used to analyze the bacterial community and abundance of phoD-harboring bacterial genes, exploring the bacterial community and abundance characteristics of phoD gene and its relationship with the forms of Po and alkaline phosphatase (ALP) activity in the soil.ResultsThe results showed that the orthophosphate monoesters (OM) were the main Po speciation and varied by P fertilization in acid purple soil. ALP activity decreased as P fertilization increased. Co-occurrence network analysis identified the overall network under five P fertilizations. The keystone taxon base on the network showed that Collimonas, Roseateles, Mesorhizobium, and Cellulomonas positively correlated with both OM and Po. The random forest showed that Cellulomonas, Roseateles, and Rhodoplanes were the key predictors for ALP activity. The keystone taxon was a more important predictor than the dominant taxon for ALP, OM, and Po. The structural equation model (SEM) showed that soil organic matter (SOM), available P (AP), and OM were the main factors influencing the ALP by reshaping phoD-harboring bacteria alpha diversity, community composition, and phoD abundance.DiscussionThe phoD-harboring bacterial community composition especially the keystone taxon rather than alpha diversity and abundance dominated the ALP activity, which could promote P utilization over an intensive agroecosystem. These findings improve the understanding of how long-term gradient fertilization influences the community composition and function of P-solubilizing microorganisms in acid purple soil.