Saline soil is a serious global environmental problem that negatively affects agricultural production because of unfavorable soil physicochemical properties and nutrient deficiencies (Shrivastava and Kumar, 2015). Accumulation of excessive sodium ions can adversely affect soil nutrient cycles (Li et al., 2016), enzyme activity (Patel and Saraf, 2013), and microbial community diversity (Bharti et al., 2016). Phosphorus (P) is one of the most important macronutrients required for plant growth. However, most P in soil is in inorganic and organic forms with low solubility that are not available for plant uptake (Adnan et al., 2017). The low availability of P in saline soil is due to fixation when P is bound to calcium (Ca), aluminum, and iron (Tchakounté et al., 2020). Salt stress can also reduce plant uptake efficiency of P, which leads to losses in crop yields (Radhakrishnan et al., 2015). To overcome P deficiency, P fertilizers can provide adequate P to increase plant productivity, although excessive application can cause eutrophication and is not economical (Park et al., 2010). Therefore, in saline soils, management must be improved to increase the availability of P and also minimize its adverse effects. In sustainable agriculture, application of biofertilizers is one potential strategy to minimize the environmental problems associated with chemical fertilizers (Chang and Yang, 2009). The use of microbial inoculation combined with rock phosphate (RP) is recognized as a suitable strategy to improve saline soil properties and plant growth (Singh and Reddy, 2011); Phosphate-solubilizing bacteria (PSB) are an integral component of the soil P cycle and play a key role in dissolving different pools of soil P to increase P availability to plants. Many PSB can significantly increase plant growth in saline soils by releasing soluble P (Ramadoss et al., 2013; Wan et al., 2020). The most effective microbes at solubilizing P include some common genera of bacteria and fungi, such as Pseudomonas, Bacillus, Micrococcus, Aspergillus, Penicillium, and Enterobacter (Ghosh et al., 2016; Ludueña et al., 2018). Moreover, halotolerant PSB can facilitate plant adaptation and tolerance to salinity stress and subsequently improve plant growth (Vassilev et al., 2006). The main mechanism underlying inorganic phosphate mineralization is the production of low-molecular-weight organic acids. These acids acidify phosphate conjugate bases, thereby increasing their solubility as a result of the reduction of soil pH, while also chelating metals (Wei et al., 2018). In our previous work, a halotolerant PSB isolated from saline soil increased the availability of nutrients to plants, and in particular soil available P. The PSB used in that study, a strain of Providencia rettgeri, may thus have potential use as a biofertilizer to sustain the growth of peanut in salt-affected soil (Jiang et al., 2019). However, few studies have explored the potential of halotolerant PSB to dissolve multiple P sources.

Rock phosphate (RP) is a raw material used in manufacturing phosphatic fertilizers; it has been used as an alternative P source extensively due to its lower cost and as a support for sustainable agriculture (Xiao et al., 2011). However, the extremely poor solubility of RP limits its direct use as a soil amendment, especially in saline–alkaline soil. Previous studies have shown that RP can improve the physicochemical properties of saline soils and that inoculation with PSB enhances the effects (Baig et al., 2010). Adnan et al. (2020) found that compared with the application of only RP, the combination of RP and PSB increases maize P acquisition under salinity stress. Most studies now focus on using the combined application of RP and PSB to increase the growth of plants and improve soil physicochemical properties (Iqbal et al., 2019). Microbial communities are an integral part of soil ecosystems and are considered the main drivers of soil fertility and quality (van der Heijden and Wagg, 2013). However, microbial populations are often restricted by nutrient deficiencies in saline soils (García-Orenes et al., 2010). The use of PSB as bioinoculants has been shown to influence microbial communities that colonize the rhizosphere and further increase soil enzyme activity and nutrient contents (Li et al., 2014). According to Song et al. (2021), PSB enhanced the abundance of beneficial microorganisms and decreased the abundance of harmful microorganisms. PSB can secrete a growth-promoting substance or release a chemical signal to promote their own growth, thereby improving relative microbiology abundance and accelerating plant uptake of nutrients from the soil. Silva et al. (2017) reported that long-term RP fertilization also changes microbial community structure, with microorganisms related to P solubilization and acquisition increasing in abundance. Therefore, PSB can be used in the form of bioinoculants in agriculture to benefit the regulation of soil microbial communities. However, the effects of the interaction between RP and halotolerant PSB on rhizosphere microbial diversity remain poorly understood.

Peanut (Arachis hypogaea L.) is an economically valuable crop. However, high salt levels and P deficiency limit peanut production and ultimately lead to severe losses in yield (Sharma et al., 2016). Information on the combined application of halotolerant PSB and RP is lacking for peanuts grown in saline soils. In addition, the effects of the combined application of halotolerant PSB and RP on saline soil microbial communities have not been investigated. Our hypothesis, therefore, was that introducing PR in conjunction with PSB inoculation to saline soils would modify their properties and bacterial community. This treatment may be useful for increasing the available phosphorus content and promoting plant growth. Thus, the primary objective of this study was to evaluate the effects of the interaction between halotolerant PSB and RP on soil properties and peanut growth in a saline soil. Changes in bacterial community structure were examined to better understand the microbiological mechanisms underlying the improvements in soil properties and plant growth.

Saline soils negatively affect plant growth because of nutrient deficiencies and salts (Yang et al., 2012). To address these problems, the combined application of RP and PSB as a potential substitute for chemical fertilizers has aroused considerable recent attention (Yadav et al., 2017). PSB play an important role in P cycling in soil–plant systems. Many PSB strains in the genera Burkholderia, Enterobacter, Paenibacillus, and Pseudomonas can potentially promote plant growth, by participating in various biological processes (Ait Barka et al., 2006). Shahzad et al. (2017) reported that the interaction between RP and PSB improved soil biochemical properties in dryland agriculture. However, the current study is the first to report that the interaction between RP and halotolerant PSB (Providencia rettgeri strain TPM23) improved soil biochemical properties and peanut production in a saline soil.

The application potential of halotolerant PSB in agriculture is based on their ability to increase crop growth and eliminate the effects of stress without harming the environment (Shukla et al., 2012). The addition of P fertilizer can strengthen the effects of PSB because it provides a substrate that benefits the proliferation and survival of inoculated PSB (Yu et al., 2011). In this study, the growth of peanut in a saline soil increased under the combined the effect of RP and PSB. Other studies also indicate that PSB combined with an insoluble phosphate source can improve plant growth and yield as well as soil conditions (Gurdeep and Reddy, 2015; Mahanta et al., 2018). Estrada et al. (2013) and Yadav et al. (2014) found similar results with tricalcium phosphate or P₂O₅ amendments. Phosphorus uptake by plants reflects P availability in various treatments. In the present study, the combined application of PSB and RP significantly increased P uptake in comparison with only RP amendment or PSB inoculation. In addition, for the treatments with combined applications of PSB and RP with an increase in peanut growth parameters, N, P, and K accumulation increased significantly in leaves. Similarly, Khosravi et al. (2018) found that the co-application of plant growth-promoting rhizobacteria (PGPR) and RP significantly increased N, P, and K uptake rates in lettuce, which led to increases in biomass and length. Thus, the inoculation of seeds with PSB combined with a mineral P source is beneficial to crop growth, regardless of the type of mineral P. The application of RP provides a nutrient substrate for PSB, and a large population of PSB can continuously dissolve the RP and release much more available P for plants, As a result, plant growth improves and biomass increases.

In addition to effects on plants, the complex interaction between PSB and RP also affects soil physicochemical properties. One of the main mechanisms leading to the dissolution of inorganic phosphate in soil is the reduction in rhizosphere pH due to the release organic acids (Rfaki et al., 2020). A small reduction in soil pH was observed with PSB inoculation or RP amendment compared with that in the control. However, the most significant reduction in pH was in the combined PSB and RP treatment. The greater reduction in pH might be because the RP was a substrate for PSB and associated with subsequent increases in microbial biomass would be increased excretion of organic acids, lowering the pH. The decrease in rhizosphere pH would then lead to the dissolution of P sources and increase the availability of P (Taktek et al., 2017). Moreover, according to Arora (2016), PSB can be used to decrease or exclude soil ions. Similarly, we found that Cl^– and Na⁺ decreased in the combined RP and PSB treatment. The decrease might be because the Ca²⁺ of RP can react with Na⁺ to form a calcium colloid, which increases the formation of soil aggregates and improves soil structure (Lebron et al., 2002; Chen et al., 2009). The solubility of the Na₂SO₄ is also greatly reduced compared with that of NaCl, which increases the salt-leaching of salinity components and inhibits soil processes. Thus, the application of RP and PSB reduced the pH while optimizing the salt–alkali ion composition. However, the content of Ca²⁺ increased with the addition of RP, likely because it was enriched with calcium ions.

Additionally, PGPR are exogenous bacteria introduced into soils to participate in soil processes such as the storage and release of nutrients (Ribeiro and Cardoso, 2012; Patel and Saraf, 2013). In this study, we found a higher level of AN, AP, and AK with PSB inoculation. Da Costa et al. (2015) also found a significantly higher level of AP when RP was combined with PSB, compared with other treatments. The PSB acidify soil by producing organic acids, which increases the solubility of P from RP (Yadav et al., 2015). In addition, PSB increases alkaline phosphomonoesterases activity to increase the solubility of P (Prabhu et al., 2018). In this study, the addition of PSB significantly affected soil enzyme activity. This result may have been related to the number and diversity of soil microorganisms, and that the metabolic activity of microorganisms can enhance soil enzyme activity. The secretion of organic acids and an increase in the root exudates can also increase soil enzyme activity. This result is consistent with that of Balota and Chaves (2010) who found that increases in soil enzyme activity are related to PGPR inoculation.

Soil microorganisms are critical to ecosystem functions and the maintenance of soil fertility. However, in saline soils, microbial populations are often restricted by nutrient deficiencies. Plant growth-promoting rhizobacteria (PGPR) are exogenous bacteria, and inoculation with PGPR can greatly affect existing soil microbial communities (Jeong et al., 2013; Bharti et al., 2015; Sheridan et al., 2017). In this study, PSB inoculation strongly increased the α-diversity of bacterial communities. Such enrichment has been attributed to increased dissolution of chemical substrates with bio-inoculation, because released nutrients are then used by resident populations to promote their growth (Bharti et al., 2015). However, the distribution of sequences demonstrated that each rhizosphere bacterial community was unique, indicating that PSB inoculation stimulated the growth of additional bacterial taxa. In this study, the phyla Proteobacteria, Acidobacteria, Actinobacteria, Chloroflexi, Bacteroidetes, Planctomycetes, and Gemmatimonadetes dominated bacterial communities. Li et al. (2016) also found that most of these bacterial phyla were dominant in saline soils. However, the structure of rhizosphere-associated bacterial communities was different among treatments in this study. The application of RP and inoculation with PSB, as well as their interaction, were responsible for the differences. These results are consistent with those of Silva et al. (2017) who found an increase in bacterial communities in soils with long-term RP fertilization. Bacterial community structure was different between treatments with and without PSB inoculation. The differences might be because PSB inoculation was the major factor in determining the structure of bacterial communities in the saline soil. Acidobacteria, Chloroflexi, and Planctomycetes were most affected by treatment and were the dominant bacterial phyla in the combined RP and PSB treatment (P < 0.05). In addition, the three phyla were significantly positively correlated with root dry weight. Thus, the inoculation of PSB combined with RP favored the establishment of three dominant bacterial phyla and further promoted peanut growth. The phylum Acidobacteria is important in nutrient turnover and is also highly involved in rhizosphere physiological processes. In addition, the abundance of the Planctomycetes increases strongly following additions of inorganic P (Ganzert et al., 2011).

Luo et al. (2017) analyzed the functional genes and bacterial community structures associated with the P cycle and found that bacteria with the alkaline phosphomonoesterases gene phoD in soil are mainly composed of Actinobacteria and Proteobacteria. In this study, Actinobacteria were enriched after inoculation with PSB, which could lead to increases in alkaline phosphomonoesterases activity and thereby increase the availability of P in the saline soil. All the above results showed that the amendments affected the abundance and diversity of bacterial communities The application of PSB significantly increased the abundance of bacteria associated with soil nutrient cycling processes, which ultimately affects the health of saline soil.

In this study, halotolerant PSB (Providencia rettgeri strain TPM23) and RP effectively alleviated salt stress in peanut in saline soil. A strong synergistic effect was found between PSB inoculation and RP amendment for promoting plant growth and soil quality as well as microbial community diversity. The application of PSB significantly increased the populations of Acidobacteria, Chloroflexi, and Planctomycetes, which are phyla involved in nutrient cycling processes that could ultimately affect the health of the saline soil. Therefore, the combination of PSB and RP might be a low-cost and environmentally safe alternative strategy to remediate the problem of low nutrient availability in saline soils.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi.nlm.nih.gov/genbank/, KX834965.

HJ and PQ designed the research. HJ and TW performed the experiment and data analysis. HJ wrote the manuscript. GC and SL participated in data download, manuscript revision, and document proofreading. XC guided the research. All the authors had read, edited and approved the final manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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