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Long-Term Organic Fertilization Strengthens the Soil Phosphorus Cycle and Phosphorus Availability by Regulating the pqqC- and phoD-Harboring Bacterial Communities

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Abstract

The pqqC and phoD genes encode pyrroloquinoline quinone synthase and alkaline phosphomonoesterase (ALP), respectively. These genes play a crucial role in regulating the solubilization of inorganic phosphorus (Pi) and the mineralization of organic phosphorus (Po), making them valuable markers for P-mobilizing bacterial. However, there is limited understanding of how the interplay between soil P-mobilizing bacterial communities and abiotic factors influences P transformation and availability in the context of long-term fertilization scenarios. We used real-time polymerase chain reaction and high-throughput sequencing to explore the characteristics of soil P-mobilizing bacterial communities and their relationships with key physicochemical properties and P fractions under long-term fertilization scenarios. In a 38-year fertilization experiment, six fertilization treatments were selected. These treatments were sorted into three groups: the non-P-amended group, including no fertilization and mineral NK fertilizer; the sole mineral-P-amended group, including mineral NP and NPK fertilizer; and the organically amended group, including sole organic fertilizer and organic fertilizer plus mineral NPK fertilizer. The organically amended group significantly increased soil labile P (Ca2-P and enzyme-P) and Olsen-P content and proportion but decreased non-labile P (Ca10-P) proportion compared with the sole mineral-P-amended group, indicating enhanced P availability in the soil. Meanwhile, the organically amended group significantly increased soil ALP activity and pqqC and phoD gene abundances, indicating that organic fertilization promotes the activity and abundance of microorganisms involved in P mobilization processes. Interestingly, the organically amended group dramatically reshaped the community structure of P-mobilizing bacteria and increased the relative abundance of Acidiphilium, Panacagrimonas, Hansschlegelia, and Beijerinckia. These changes had a greater positive impact on ALP activity, labile P, and Olsen-P content compared to the abundance of P-mobilizing genes alone, indicating their importance in driving P mobilization processes. Structural equation modeling indicated that soil organic carbon and Po modulated the relationship between P-mobilizing bacterial communities and labile P and Olsen-P, highlighting the influence of SOC and Po on the functioning of P-mobilizing bacteria and their impact on P availability. Overall, our study demonstrates that organic fertilization has the potential to reshape the structure of P-mobilizing bacterial communities, leading to increased P mobilization and availability in the soil. These findings contribute to our understanding of the mechanisms underlying P cycling in agricultural systems and provide valuable insights for enhancing microbial P mobilization through organic fertilization.

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Data Availability

The raw sequences of pqqC- and phoD-harboring bacterial were deposited in the National Center for Biotechnology Information Sequence Read Archive database with the sample accession PRJNA956135.

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Acknowledgements

We thank International Science Editing (https://www.internationalscienceediting.com) for editing this manuscript.

Code Availability

This study does not include any software application or custom code.

Funding

This study was financially supported by the Natural Science Foundation of Jiangsu Province (BK20190259), the earmarked fund for CARS-10-Sweetpotato, the Key Research and Development Project of Jiangsu Province (BE2021378), the Jiangsu Agriculture Science and Technology Innovation Fund (CX(21)1009), and “1+1+N” Innovative Agricultural Technology Extension Project of Zhenjiang (ZJNJ[2021]04).

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Authors and Affiliations

  1. Institute of Agricultural Resources and Environment, Jiangsu Academy of Agricultural Sciences/National Agricultural Experimental Station for Agricultural Environment, Luhe, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China

    Lei Wang, Jie Yuan, Jidong Wang & Yongchun Zhang

  2. Xuzhou Institute of Agricultural Sciences of Xuhuai District of Jiangsu Province, Xuzhou, 221131, China

    Jing Wang & Zhonghou Tang

Authors
  1. Lei Wang
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  2. Jing Wang
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  3. Jie Yuan
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  4. Zhonghou Tang
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Contributions

Lei Wang: methodology, investigation, data analysis, and writing—original draft preparation and editing. Jing Wang and Jie Yuan: collecting samples, performing experiments, and editing manuscript. Zhonghou Tang: experiment design, investigation, and review and editing. Jidong Wang and Yongchun Zhang: investigation, funding support, supervision, and editing manuscript.

Corresponding authors

Correspondence to Jidong Wang or Yongchun Zhang.

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Supplementary Information

ESM 1

Fig. S1 Proportions of organic P and each inorganic P fractions for different fertilization regimes. CK, no fertilizer; NK, inorganic NK fertilizer; NP, inorganic NP fertilizer; NPK, inorganic NPK fertilizer; M, organic fertilizer; NPKM, inorganic NPK plus organic fertilizer. (PNG 46 kb)

ESM 2

Fig. S2 Pearson’s correlation among soil P fractions and Olsen-P (A). Random forest analysis to identify the relative effects of soil P fractions on Olsen-P (B). (PNG 307 kb)

ESM 3

Fig. S3 Principal coordinate analysis based on Bray–Curtis distance was used to investigate the community structure of pqqC- and phoD-harboring bacteria in different fertilization treatments (A). Hierarchical clustering based on unweighted Unifrac distance to explore the community structure of pqqC- and phoD-harboring bacteria in soil under different fertilization treatments (B). CK, no fertilizer; NK, inorganic NK fertilizer; NP, inorganic NP fertilizer; NPK, inorganic NPK fertilizer; M, organic fertilizer; NPKM, inorganic NPK plus organic fertilizer. (PNG 608 kb)

ESM 4

Fig. S4 Structure equation model of the phoD-harboring bacteria genera and labile Po (A) or ALP (B) under the influence of soil Po. Structure equation model of the pqqC-harboring bacteria genera and labile Pi under the influence of SOC (C). Po, Organic P; ALP, Alkaline phosphomonoesterase; SOC, Soil organic carbon. (PNG 716 kb)

ESM 5

Fig. S5 Effects of different long-term fertilization treatments on sweetpotato yield. Different letters indicate significant difference at P < 0.05. CK, no fertilization; NK, mineral NK fertilizer; NP, mineral NP fertilizer; NPK, mineral NPK fertilizer; M, sole organic fertilizer; NPKM, organic fertilizer plus mineral NPK fertilizer. (PNG 51 kb)

ESM 6

Table S1 Inorganic and organic fertilizer application rates in different long-term fertilization regimes (DOC 37 kb)

ESM 7

Table S2 Pearson’s correlation coefficients among soil physicochemical, the pqqC- and phoD-harboring bacterial community diversity (DOC 35 kb)

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Wang, L., Wang, J., Yuan, J. et al. Long-Term Organic Fertilization Strengthens the Soil Phosphorus Cycle and Phosphorus Availability by Regulating the pqqC- and phoD-Harboring Bacterial Communities. Microb Ecol 86, 2716–2732 (2023). https://doi.org/10.1007/s00248-023-02279-7

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