Partial replacement of inorganic phosphorus (P) by organic manure reshapes phosphate mobilizing bacterial community and promotes P bioavailability in a paddy soil

https://doi.org/10.1016/j.scitotenv.2019.134977Get rights and content

Highlights

  • Combination of mineral P and manure increased phoD gene abundance and P availability.

  • The reducing P input enriched the abundance of Bradyrhizobium and Methylobacterium.

  • P mobilizing communities were primarily driven by soil pH to enhance P mobilization.

Abstract

The optimization of more sustainable fertilization practice to relieve phosphorus (P) resource scarcity and increase P fertilizer utilization, a better understanding of the regulatory roles of microbes in P mobilization is urgently required to reduce P input. The genes phoD and pqqC are responsible for regulating organic and inorganic P mobilization, respectively. Using high-throughput sequencing, the corresponding bacterial communities harbored by these genes were determined. We conducted a 4-year rice-rice-crop rotation to investigate the responses of phoD- and pqqC-harboring bacterial communities to the partial replacement of inorganic P fertilizer by organic manure with reduced P input. The results showed that a combination of organic and inorganic fertilization maintained high rice yield, and also produced a more complex and stable phosphate mobilizing bacterial community, which contributed to phosphatase activities more than their gene abundances in the model analysis. Compared with the conventional mineral fertilization, organic-inorganic fertilization with the reduced P input slightly increased pqqC gene abundance while significantly enhanced the abundance of phoD-harboring bacteria, especially the genera Bradyrhizobium and Methylobacterium known as potential organic P mineralizers which can maintain high rice production. Moreover, the increased pH was the most impactful factor for the phoD- and pqqC-harboring bacterial communities, by promoting microbial P turnover and greatly increasing bioavailable P pools (H2O-Pi and NaHCO3-Pi, NaOH-Pi) in this P-deficient paddy soil. Hence, our study demonstrated that the partial replacement of mineral P with organic manure could reshape the inorganic phosphate solubilizing and alkaline-phosphomonoesterase encoding bacterial communities towards more resilient and effective to the high P utilization and productivity over intense cultivation, providing insights into the potential of soil microbes in the efficient management of agricultural P fertilization.

Introduction

Phosphorus (P) is a critical nutrient for plant growth, but its availability is mostly limited in agro-ecosystems worldwide (George et al., 2017). Thus, mineral P with high input is continuously applied to the soil to maintain high crop yields. However, P fertilizer is easily fixed in soils rather than absorbed by plants (Kochian, 2012), and then an extra P fertilizer beyond the crop demand, is further applied. This can leave the continuous accumulation of soil residual P and potential eutrophication of surface water (Powers et al., 2016). The global reserves of mineral P are estimated to be 100% depleted by 2100 (Penuelas et al., 2013). Thus, the eco-friendly fertilization management for decreasing P usage and improving P use efficiency is urgently needed for both agricultural production and environmental health.

Organic fertilization, which better supports soil fertility and quality, is becoming a feasible practice to maintain high crop yield to meet the ever-increasing food demand for the booming global populations (Sun et al., 2015). Long-term organic fertilization (e.g., dry straw, animal manure, among others) is beneficial for plant-available P supplies, soil quality improvement, and P-related enzyme activities (Steiner et al., 2007, Zhu et al., 2010). Additionally, P sourced from manure is more likely to remain available forms than that from chemical fertilizers, causing a better plant uptake (Kahiluoto et al., 2015). Moreover, chemical fertilization over decades may further decrease potential alkaline phosphatase (ALP) activity (Fraser et al., 2015a). The combined application of organic and inorganic fertilizer greatly increases ALP activity, and soil P availability (Chen et al., 2017), and the increased soil organic carbon (C) content and aggregation improve environmental conditions for soil microbial community (Lin et al., 2019). Furthermore, a reduction in chemical fertilization supplemented with organic applications, possibly enhances soil microbial nutrient cycling (Ding et al., 2018). For example, comparing to the conventional chemical fertilization, reducing nitrogen (N) or chemical fertilizer input coupled with organic amendments can strengthen soil nitrification and N fixation with the increase in N utilization efficiency and crop productivity (Hsu and Buckley, 2009, Zhao et al., 2016). Accordingly, reducing mineral P input combined with organic-inorganic fertilization is expected to produce higher efficient soil P mobilization and cycle, which is necessary to enhance P fertilizer utilization and then the environmental sustainability of crop production.

Microbial community diversity and compositions can be greatly altered by agricultural activities, with consequent effects on the biogeochemical cycles mediated by microorganisms (Zhu et al., 2017). One positive feedback is the regulation of plant P acquisition by solubilizing insoluble P with organic protons or mineralizing recalcitrant organic-P with enzymes (Richardson and Simpson, 2011). The gene encoding pyrroloquinoline-quinone involved in gluconic acid production for inorganic-P release, a potential bioindicator for inorganic phosphate solubilizing bacteria (iPSB) communities (Rodríguez et al., 2006), was previously used in a long-term fertilized soil (Zheng et al., 2017). The putative Pho regulon genes (phoA, phoD, and phoX) are responsible for alkaline phosphatase expression in soil and aquatic ecosystems (Chen et al., 2017, Hu et al., 2018, Ragot, 2016). While phoD is dominant in soil and can provide evidence for organic P transformation (Chen et al., 2017, Ragot et al., 2016, Tan et al., 2012). Several studies indicated that different fertilizing strategies altered the phoD-harboring bacterial community composition and diversity with the potential effects on organic P mineralization, but responses were inconclusive, which is probably due to the various soils and organic fertilizer types and also the different P statuses (Chen et al., 2017, Fraser et al., 2015b, Hu et al., 2018, Tan et al., 2012). For example, the phoD gene abundance and diversity were decreased when chemical fertilizer added with corn straw but increased in combination with swine manure in a red soil (Chen et al., 2017). In a calcareous soil, only organic fertilization combinations with high amounts of organic matter significantly affected the phoD gene abundance and community, however, the soil organic mineralization in different treatments was benefited from the abundant phoD-harboring taxa (Hu et al., 2018). However, in the mineral P-fertilized paddy soil, rare phoD-harboring taxa were found to contribute to the increase in phoD gene abundance (Wei et al., 2019). Thus, more studies on the alkaline-phosphomonoesterase encoding bacterial community in different soils or fertilization management are needed. Moreover, after long-term organic-inorganic fertilization, some specific microbial taxa were found to be more effective in the decomposition of complex organic matter and soil C, N, and P transformation (Gu et al., 2017, Li et al., 2017). However, the major studies of P mobilizing bacterial community are based on the phosphomonoester mineralization, little is known about the combined role of the alkaline-phosphomonoesterase encoding and phosphate solubilizing bacterial communities on the P mobilization, especially in paddy soils with the partial replacement of mineral P by organic manure.

In this study, a rice-rice field cropping over 4 years in southern China was conducted to investigate the effects of various fertilizing strategies, including the conventional chemical, organic, and combinations of organic-inorganic fertilization with or without reducing mineral P input on phoD- and pqqC-harboring bacterial communities. We hypothesized that different fertilization regimes could change soil P pool distribution, the abundance and compositions of the alkaline-phosphomonoesterase encoding and phosphate solubilizing bacterial communities, particularly the partial replacement of inorganic fertilizer by organic manure would facilitate the potential phosphatase activity and P availability by establishing a better phosphate mobilizing bacterial community, even while reducing P input. Due to the complexity of soil microbial interactive webs, network analysis and structural equation models (SEM) are introduced to comprehensively understand the relationships between soil properties, phoD- and pqqC-harboring communities, and their functionality, to explore how the phosphate mobilizing bacterial community is driven.

Section snippets

Field design and soil sampling

The field was located in Yichun, Jiangxi, China (28°15′1.62″N, 115°07′13.34″E). This region has a subtropical monsoon-type climate with an average annual temperature of 17.2 °C and average annual precipitation of 1,680 mm. The red soil had the following basic properties: pH 5.4; total organic C 16.3 g kg−1; total N 1.1 g kg−1; total potassium (K) 21.1 g kg−1; total P 0.6 g kg−1; and available P 23.8 mg kg−1. To accomplish the aim of “Zero Increase Action Plan” in China by 2020 Liu et al. (2016)

Soil properties and P status

The selected biological and chemical characteristics of soil samples are presented in Table 1. Soil SOC, pH, Pt, NO3, Posl contents, and ACP, ALP, and PDE activities were significantly increased after 4-year conventional (FP treatment) and organic-inorganic fertilization (CMP and CM(-P) treatments) compared with the other treatments (P < 0.05). Moreover, in comparison with conventional fertilization, organic-inorganic fertilization significantly enhanced the Posl, NH4+ contents, and ACP

Discussion

In the acidic paddy soil, low P availability is the major limitation of crop production. Thus, fertilization is the most common agricultural management practice for improving soil P fertility, mainly through the amendment of mineral P or organic manure (Ai et al., 2018, Hu et al., 2018, Zhao et al., 2016). In the current study, compared with the single organic manure fertilized soil (M(20%P) treatment) and the Non-P fertilized soils (the control and NK treatments), the conventional chemical

Conclusions

In this study, a 4-year field experiment demonstrated that organic-inorganic fertilization with reduced P input significantly enhanced soil P availability and maintained high rice yield in comparison with conventional fertilization. Different fertilization regimes notably reshaped the abundance and composition of phoD- and pqqC-harboring bacterial communities, which was of higher network complexity and stability with the 4-year organic-inorganic fertilization. Moreover, the continued reduction

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We thank Huang-Kai Zhang for the sequencing data blast. This work was financially supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB 15020402 and XDB 15020302) (China), and the National Key Research and Development Program of China (No. 2017YFD0200201) (China). QFB would like to acknowledge the China Scholarship Council.

Author contributions

All authors contributed the intellectual input and assistance to this study and manuscript preparation. XYL conceived and designed the study. QFB and KJL collected the samples. QFB did the experiments with help from XPL, HZL and BJJ. QFB performed data analysis, with help from KD and XRY. QFB wrote the paper. YGZ, XYL and BXZ revised the manuscript. All authors read and approved the final manuscript.

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    Qing-Fang Bi and Ke-Jie Li contributed equally to this work.

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