This study investigated the shifts in the community composition and co-occurrence networks of soil microbiota in relation to the soil ionome in a kiwifruit orchard under different fertilization regimes. A 9-year split-plot field experiment (2009–2018) was conducted in Meixian county, Shaanxi province, China. Two main plots were assigned to bio-organic fertilization (0 vs. 8000 kg ha−1 y−1), each containing two subplots assigned to chemical fertilization (0 vs. 300 kg N ha−1 y−1, 225 kg P ha−1 y−1, and 150 kg K ha−1 y−1). High-throughput sequencing and inductively coupled plasma-mass spectrometry were used to analyze soil microbial community composition and ion concentrations, respectively. Results showed that bio-organic fertilization increased soil Ni, Se, total C, total N, and pH levels, whereas soil Mg, Cu, Zn, and Sr concentrations were decreased. Mantel testing indicated that bacterial community composition was influenced more easily by the availability of soil ions (e.g., Zn, Ni, Co, Cu) than fungal community composition. Bio-organic fertilization also increased bacterial α-diversity indices that were strongly correlated with the availability of soil ions (e.g., Fe, Mn, and Ca). Network analysis revealed that bio-organic fertilization generated more links (especially positive links) between microbial taxa in the community. Fewer but highly interconnected modules were found in the network formed under bio-organic fertilization, for which fewer nodes and negative links occurred concurrently. After selecting putative keystone species, the network with bio-organic fertilization was characterized by more generalists than the network without bio-organic fertilization. In contrast to the network without bio-organic fertilization, none of the generalists in the network with bio-organic fertilization were correlated with soil total C and N contents; however, high correlations were found with soil ions (e.g., Fe, Mn, Co, and Al). These results demonstrate that a better-organized and more stable network of soil microbial communities can assemble in a kiwifruit orchard under bio-organic fertilization, as mediated by alterations to the soil ionome. This study highlights that the less-commonly researched soil ions (e.g., Ni, Mo, Se, Sr) may play a crucial role in the response of soil microbial communities to bio-organic fertilization in agricultural ecosystems.
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