The alkaline phosphomonoesterase (ALP)-harboring community (phoD-harboring community) plays a crucial role in the conversion of organic phosphorus (P) into available P (AP). However, the response mechanisms of phoD-harboring communities to fertilization strategies, crop types, and their interactions within the wheat-sweetpotato rotation are poorly understood. A nine-year field experiment of different fertilization strategies was established under the wheat-sweetpotato rotation. After harvesting the crop, we collected soil samples without fertilization (CK), inorganic NK fertilization (NK), inorganic NPK fertilization (NPK), and a combined application of inorganic NPK and organic fertilizer (NPKM). We employed high-throughput sequencing and enzymology techniques to analyze the composition and functional activity of phoD-harboring bacterial communities as well as their correlation with soil physicochemical properties. The results showed that long-term nitrogen (N) fertilization, especially inorganic N, significantly reduced soil pH and ALP activity while increasing AP compared with CK. The AP content in sweetpotato season was significantly higher than that in wheat season. Inorganic N fertilization dramatically reshaped the communities of phoD-harboring bacteria and decreased diversity. The phoD-harboring bacterial communities in sweetpotato season were significantly different from those in wheat season. The N fertilization significantly reduced the relative abundance of Acuticoccus, Methylibium, Rhizobacter, and Roseivivax, which was positively correlated with ALP activity. These groups in sweetpotato season decreased significantly compared with wheat season. A structural equation model indicates that pH and AP play a significant role in regulating the phoD-harboring bacteria communities, ALP activity, and their interactions. We demonstrate that fertilization strategies and crop types have a substantial impact on the phoD-harboring bacteria communities and functions, which are closely linked to soil pH and AP levels. Our study highlights the detrimental effects of soil acidification resulting from inorganic N fertilization on P-cycling bacterial communities and functions. However, the combination of inorganic and organic fertilizer can mitigate these adverse effects.
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