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Chemical and Biological Technologies in Agriculture
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Phosphorus-, potassium-, and silicon-solubilizing bacteria from forest soils can mobilize soil minerals to promote the growth of rice (Oryza sativa L.)

Chemical and Biological Technologies in Agriculture volume 11, Article number: 103 (2024) Cite this article

Abstract

Background

Forest soils are usually highly weathered and abundant in mineral-weathering bacteria, which have not been used to mobilize soil minerals for crop production. Here, we used an acidic forest soil with low available phosphorus (P), potassium (K), and silicon (Si) to isolate bacteria capable of co-solubilizing P, K, and Si (PKSi-solubilizing) and the model rice plant to test their potential to mobilize soil P, K, and Si for crop nutrition.

Results

Six PKSi-solubilizing strains representative of common mineral-weathering proteobacteria taxa (genera Burkholderia, Paraburkholderia, Collimonas, Pseudomonas, and Agrobacterium) were screened out. They showed diverse P-, K-, or Si-solubilizing activities and produced diverse organic acids. Their mineral-solubilizing activities were positively correlated with the levels of medium pH reduction and gluconic acid production. They promoted the growth of rice seedlings grown in the forest soil by increasing soil available P and Si, plant P, K, and Si cumulative contents and dry weight, and the corresponding root-to-shoot ratios. The growth of rice seedlings alone and with the inoculated PKSi-solubilizing stains in the acidic forest soil did not reduce the soil pH.

Conclusions

The forest soil with low available P, K, and Si is a valuable resource for high-performance PKSi-solubilizing bacteria improving soil fertility and crop nutrition. The PKSi-solubilizing bacteria screened out can promote rice seedling growth by mobilizing P, K, and Si from soil to plant in the acidic soil with low available P, K, and Si. They show potentials to mitigate soil P, K, and Si deficiency and promote crop growth, and to recover soluble P, K, and Si from chemical fertilizers and improve the use efficiency of chemical fertilizers, thus reducing the input of chemical fertilizers. They may retard soil acidification by Si-solubilization and improve soil quality.

Graphical Abstract

Highlights

  • Forest soils with low available P, K, and Si are resources of PKSi-solubilizing bacteria.

  • PKSi-solubilizing bacteria at high abundance in soils are representative of common mineral-solubilizing taxa.

  • PKSi-solubilizing bacteria promote crop growth via mineral-mobilization from soils to plants.

  • PKSi-solubilizing bacteria produce organic acids to solubilize P, K, and Si.

  • Si-solubilization may neutralize soil acidification.

Introduction

Phosphorus (P) and potassium (K) are finite and nonrenewable resources and are essential macronutrient elements for plant growth and development [1, 2]. Silicon (Si) is present in plants in amounts equivalent to those of macronutrient elements, especially in plants within family Poaceae and deemed a “quasi-essential” element for plant growth, development, and resistance to various abiotic and biotic stress [3,4,5,6]. Particularly, rice, a typical Si-accumulating Poaceae plant, accumulates the highest Si content up to 10% of the shoot dry weight and benefits from Si nutrition [4,5,6].

Despite that P, K and Si are present in large amounts in natural soils, only a small proportion is readily available to plants [3, 7, 8]. To crops, most nature soils are P and K deficient. Substantial chemical P and K fertilizers have been applied to agricultural soils to gain desirable yield of crops. However, long-term use of P and K fertilizers has been accompanied by the reduction of the fertilizer use efficiency [8, 9]. Particularly, because of the high reactivity of P with some metals, such as calcium (Ca), iron (Fe), and aluminum (Al), a large portion of P in the fertilizers are converted to insoluble phosphate and metal complexes and become unavailable to crops [7]. Moreover, a proportion of the applied P and K fertilizers has been lost from agricultural soils to water bodies, causing adverse environmental impacts [1, 2]. A solution for effective use the insoluble P and K resources in natural soils and the applied P and K fertilizers is adding P and K solubilizers in the soils and fertilizers [2, 7, 9,10,11,12,13].

Microbial weathering of P-, K-, and Si-bearing minerals done by a wide range of saprophytic bacteria, actinomycetes, and fungi is a major source of available P, K, and Si for plants [2, 7, 9,10,11,12,13,14,15,16]. The general mineral-solubilizing process involves dissolution and desorption driven by interrelated mechanisms of acidification, chelation, and exchange reactions [15,16,17]. The acidification or acidolysis directly dissolving the minerals is driven by microbial production and release of protons (H+), organic acids, and inorganic acids, thereby decreasing soil pH surrounding the microorganisms. Chelation or complexation of metal cations, such as Fe2+, Ca2+, Al3+, and Si4+, associated with P, K, or Si minerals is driven by microbial production and release of chelating metabolites and ligands, such as organic acids and siderophores, making P, K, and Si available. Exchange reactions release soluble P (orthophosphate anions, i.e., H2PO4− and HPO42−), K+, and Si4+ from the cation-exchange complex. Some mineral-solubilizing microorganisms produce polymers, such as exopolysaccharides adsorbing and linking the chemicals, providing frameworks to facilitate the mineral solubilization [13,14,15,16]. In addition, mineral-solubilizing microorganisms produce enzymes to dissolve insoluble minerals, such as non-specific acid phosphatases in solubilizing P and Si [9, 18].

Forest soils are nature soils with undisturbed organic layers and characterized by vertical stratification resulting from the decomposition of litter-derived organic matter and the weathering of mineral matrix [19]. Forest soils rich in high organic matter are hot spots of microbial activities compared with those of agricultural soils with long-term plantation and fertilization and are among the most diverse microbial habitats on Earth, in which bacteria are the most abundant microorganisms [19, 20]. Many DNA-based analyses showed the high diversity and complex structure of bacterial communities in forest soils and the ecological roles and contributions of individual bacterial taxa to biogeochemical processes [19,20,21], such as the mineral-weathering process [17, 22,23,24,25]. Forest soils are usually highly weathered and abundant in mineral-weathering bacteria [19, 22, 25]. However, the bioresource of mineral-weathering bacteria in forest soils is rarely used to mobilize soil minerals for crop production.

In forest soils of the subtropical regions in China, the concentrations of available P (AP), available K (AK), and available Si (ASi) are highly variable while the average AP, AK, and ASi concentrations are 6.68, 100.21, and 79.8 mg kg−1, respectively [26, 27]. Generally, in the subtropical forest soils, plants have sufficient AK but insufficient AP and ASi for growth [25, 26] and suffer from soil acidification (pH value < 5.0) probably due to frequent acid precipitation and high soil organic matters [26, 28]. In agricultural soils of the same subtropical regions in China, soil acidification resulted from the high nitrogen fertilizer inputs and the increasing nitrogen deposition has become a general problem for crop production [29]. In paddy fields, chemical fertilization and intensive cultivation have led to increased soil AP but decreased AK and ASi, which are associated with annual removal of straws and husks containing K and Si [30,31,32]. On the other hand, long-term continuous application of Si fertilizer can increase paddy soil pH [33], and fertilization of silica rock along with Si-solubilizing bacteria can promote rice growth and increase soil pH [34]. Therefore, application of silica rock along with Si-solubilizing bacteria may be a solution to retard soil acidification and counteract the side effect of the acidification-directed mineral weathering in soils.

Growing evidence supports that application of biofertilizers containing P-, K-, and Si-solubilizing bacteria in agricultural soils deficient in available P, K, and Si can disintegrate P-, K-, and Si-bearing minerals and release soluble P, K, and Si into the soil solution, supplying P, K, and Si nutrients to plants [9,10,11,12,13,14,15,16]; application of P, K, and Si rocks along with P-, K-, and Si-solubilizing bacteria can be a cost-effective, environment-friendly and long-term strategy to reduce the inputs of chemical fertilizers, increase mineral use efficiency, reduce soil acidification for sustainable agriculture [2, 9,10,11,12,13,14,15,16, 34].

The high abundance of mineral-solubilizing bacteria in mineral-poor soils is under a selection pressure of low mineral availability [24, 35]. The abundant mineral-weathering bacteria in highly weathered forest soils are the potential bioresources for the application of P, K, and Si biofertilizers in agricultural soils. In this study, we chose an acidic forest soil containing very low levels of AP, AK, and ASi from a subtropical region in Zhejiang Province, southeastern China to isolate and screen bacteria at high abundance in the soil and capable of co-solubilizing P, K, and Si (PKSi-solubilizing bacteria) and used the model rice plant to test their potential to supply P, K, and Si to crop plants and explore the bioresource of PKSi-solubilizing bacteria in forest soils for improving soil fertility and crop production.

Materials and methods

Soil

The forest soils were collected from an evergreen broadleaf forest (119° 39′ 77.898ʺ E, 30° 12′ 91.982ʺ N, 80.0 m above sea level) at the Yiwu Village, Lin’an District, Hangzhou, Zhejiang Province, China, on 2021-09-20. Three 100 m2 squares were randomly selected and five soil columns were collected from the top layer (0‒15 cm). The soils from the three squares were thoroughly mixed while plant roots and debris in the soils were removed via a 2-mm mesh sieve. We stored 1 kg of the soil in sterile bags at 4 °C for screening of mineral-solubilizing bacteria with the remaining soil air-dried. About 1 kg of the air-dried soil was subjected to physicochemical analyses. The soil contained 4.9 mg kg−1 of AP, 34.5 mg kg−1 of AK, and 23.0 mg kg−1 of ASi, 38.4 g kg−1 soil organic matter, 468.2 mg kg−1 of soluble organic carbon, 29.2 mg kg−1 of nitrate nitrogen, and 31.6 mg kg−1 of ammonium nitrogen while the soil pH was 4.95 ± 0.03. This soil is a typical acidic subtropical forest soil containing very low levels of AP, AK, and ASi [26, 27].

Screening of PKSi-solubilizing bacteria

The soil stored at 4 °C for 7 d was used to isolate PKSi-solubilizing bacteria. Ten grams of the soil was added into 90 mL of sterile water in a 250-mL Erlenmeyer flask and was shaken at 180 rpm and 28 °C for 30 min. Afterwards, 10 mL of the soil suspension (about 1 g soil per 10 mL) was added into 90 mL of sterile water in a 250-mL Erlenmeyer flask and was shaken at 180 rpm and 28 °C for 3 min. This tenfold dilution was serially done six times to a final dilution of 1 × 10−6. Then, 100 μL of the final diluted soil suspension was spread onto the modified solid NBRIP medium [36] containing the pH indicator bromothymol blue (NBRIP-BTB medium) [per liter: glucose 10 g; (NH4)2SO4 0.1 g; KCl 0.2 g; MgCl2·6H2O 5 g; MgSO4·7H2O 0.25 g; Ca3(PO4)2 5 g; bromothymol blue 0.025 g; agar 15 g; pH 7.5 after autoclaving]. This process was done with six replications. The NBRIP-BTB medium in 90-mm Petri dishes was incubated at 28 °C for 7 d and observed daily. Bacterial colonies turned the color of bromothymol blue from blue to yellow, and generated clear rings around the colonies were P-solubilizing bacteria abundant in the soil and then were purified by streaking on the NBRIP-BTB medium. The purified P-solubilizing bacterial colonies were cultured in liquid LB medium (per liter: tryptone 10 g, yeast extract 5 g, NaCl 10 g, pH = 7) at 28 °C and 200 rpm to OD600 (optical density at 600 nm)> 1; the cultures were then frozen with 15% (v/v) glycerol at −80 °C for long-term storage.

The purified P-solubilizing bacterial isolates were further screened for K- and Si-solubilizing activities by streaking the purified colonies on a NBRIK-BTB medium [per liter: glucose 10 g; (NH4)2SO4 0.1 g; MgCl2·6H2O 5 g; MgSO4·7H2O 0.25 g; Na2HPO4 0.2 g; K-feldspar (K2O·Al2O3·6SiO2) 10 g; bromothymol blue 0.025 g; agar 15 g; pH 7.5 after autoclaving] modified from the NBRIP-BTB medium and a Si-BTB medium [per liter: glucose 10 g; magnesium trisilicate (Mg2O8Si3) 2.5 g; bromothymol blue 0.025 g; agar 15 g, pH 7.5 after autoclaving] modified from the silicate medium described by Kang et al. [34]. The isolates that could grow on the NBRIK-BTB medium and the Si-BTB medium, turned the color of the NBRIK-BTB medium from blue to yellow, and generated clear rings around the colonies in the Si-BTB medium were screened out as PKSi-solubilizing bacteria.

Qualitative assays of bacterial P-, K-, and Si-solubilizing activities

To qualitatively compare the P-, K-, and Si-solubilizing activities of different isolates, the isolates were grown in liquid LB medium, washed with sterile water, and adjusted with sterile water to a suspension at about 1 × 109 CFU mL−1 (OD600 = 1); 10 μL of the suspension was dropped onto the center of the NBRIP-BTB, NBRIK-BTB, and Si-BTB media in 90-mm Petri dishes and incubated at 28 °C for 7 d. The clearance and size of the clearing ring around the colonies was the indicator for the P-, K-, and Si-solubilizing activities.

Quantitative assays of bacterial P-, K-, and Si-solubilizing activities

To compare the P-, K-, and Si-solubilizing activities of different isolates, the isolates were grown in the liquid NBRIP-BTB, NBRIK-BTB, and Si-BTB media. Ten milliliters of a bacterial suspension about 1 × 109 CFU mL−1 was added into 90 mL of the liquid NBRIP-BTB, NBRIK-BTB, or Si-BTB medium in a 250-mL Erlenmeyer flask and was shaken at 180 rpm and 28 °C for 7 d. Sterile water (10 mL) mixed with the 90 mL media was used as control. At 3 d and 7 d after inoculation, the pH values of the liquid media were measured using a PB-10 pH meter (Sartorius, Goettingen, Germany). At 7 d after inoculation, the supernatant of the bacterial culture was obtained after centrifugation and used to determine AP, AK, and ASi concentrations. AP was measured using the molybdenum blue colorimetric method; AK was measured using the flame photometric method; ASi was measured using the silicon–molybdenum blue colorimetric method [37]. These assays were done with three replications and repeated three times.

Quantitative analyses of bacterial production of organic acids

Organic acids in the supernatant from the 7-d bacterial cultures in the liquid NBRIP-BTB medium were determined using high-performance liquid chromatography (HPLC). The supernatant was filtered through a 0.45-μm Millipore filter. Organic acids in the filtrate were separated through a high-purity silica gel-based liquid chromatography column (Athena C18-WP, 4.6 × 250 mm, 3 μm). For gluconic acid, the mobile phase contained a 10 mmol L−1 KH2PO4–5 mmol L−1 tetrabutylammonium hydrogen sulfate aqueous solution (pH 7.0) and methanol at the volume ratio 98:2. For other 12 organic acids, the mobile phase contained a 20 mmol L−1 Na2HPO4 aqueous solution at pH 2.35 adjusted by phosphoric acid. The column temperature was 30 °C, the flow rate was 0.7 mL min−1, and the UV detection wavelength was 210 nm. Using a U3000 HPLC system (ThermoFisher Scientific, Cleveland, USA), the retention times of the standard organic acids were determined: gluconic acid 6.057 min; oxalic acid 4.487 min, tartaric acid 5.336 min, formic acid 5.605 min, pyruvic acid 6.406 min, malic acid 7.036 min, malonic acid 7.639 min, lactic acid 8.319 min, acetic acid 8.827 min, citric acid 14.219 min, succinic acid 15.497 min, fumaric acid 17.249 min, and propionic acid 21.811 min.

Culture of rice seedlings in the forest soil with PKSi-solubilizing bacteria

Seeds of the rice (Oryza sativa ssp. japonica) cultivar Nipponbare were surface-sterilized with 70% ethanol for 30 s and 3% (v/v) sodium hypochlorite (100 mL) in a 250-mL Erlenmeyer flask with shaking at 150 rpm for 10 min, and washed six times with sterile water. The surface-sterilized seeds were soaked in sterile water at 37 °C overnight to promote germination. Then, the seeds (one seed per milliliter) were soaked in an aqueous bacterial suspension about 1 × 108 CFU mL−1 (OD600 = 0.15) at 28 °C for 2 h. Seeds soaked in sterile water at 28 °C for 2 h without bacterial inoculation were used as control. Afterwards, the seeds were transferred onto a wetted sterilized filter in a 150-mm Petri dish (50 seeds per dish) and germinated at 28 °C for 2 d.

The forest soil sieved through a 2-mm mesh sieve and air-dried for 2–5 months was filled in plastic cups with a bottom hole. Each plastic cup was filled in 500 g of the soil and supported by a Petri dish bottom; the soil was inoculated with 50 mL of a bacterial suspension about 1 × 108 CFU mL−1. The germinated rice seeds inoculated with a PKSi-solubilizing bacterial strain were sown under the soil surface. The inoculated rice seedlings (3 seedlings pot−1) were grown at 26 °C under a 12-h light and 12-h dark period and watered with 50 mL of sterile ion-free water every time when needed. The soil without bacterial inoculation and planted with non-inoculated seeds was used as the non-inoculation control. The soil without plants and bacterial inoculation was used as blank control. At 7 d after sowing, one weak seedling was removed from each pot. At 35 d after sowing, rice seedlings were harvested, and plant height, root length, and dry weight of seedling shoots and roots were measured. Total P, total K, and total Si cumulative contents in the rice plants were determined using the molybdenum blue colorimetric method, the flame photometric method and the silicon–molybdenum blue colorimetric method, respectively [37]. This experiment was done with six replications and repeated three times.

Amplification and analyses of bacterial 16S rRNA gene (rrs) sequences

The 16S rRNA gene (rrs) sequences of the PKSi-solubilizing bacteria were amplified from colonies by PCR using the universal primers 27F and 1492R as previously described [38]. The amplicons were sequenced using the Sanger method and the sequences were identified using the EzBioCloud identification service (https://www.ezbiocloud.net/identify) [39]. Their rrs sequences and rrs sequences of the type strains of closely related species were aligned using the MUSCLE program integrated in the MEGA5 software [40]. After eliminating positions containing gaps and missing nucleotides at both ends of the aligned sequences, 1345 final aligned nucleotides were constructed to a phylogenetic tree using the maximum likelihood method; the evolutionary distances were computed using the Tamura–Nei model and Gamma distribution.

Statistical analysis

The data were subjected to statistical analysis using Microsoft Excel 2019 and R software (R Core Team, 2023). Analysis of variance (one-way ANOVA) followed by the least significant difference (LSD) test at the probability level of p < 0.05. The graphical representations of the data were created using GraphPad Prism 9 (GraphPad Software, Santiago, USA) and Microsoft PowerPoint 2019.

Results

Six PKSi-solubilizing isolates were screened out

Bacterial colonies appeared on the NBRIP-BTB medium from the 100-μL soil suspension diluted to 10–6 showed an abundance in the soil at least 1 × 107 CFU g−1 soil. Among the 54 bacterial colonies appeared on the NBRIP-BTB plates from the soil suspension diluted to 10–6, 45 colonies (83%) turned the color of bromothymol blue from blue to yellow around the colonies while 28 colonies (52%) also generated clear rings around the colonies and were considered as P-solubilizing bacteria abundant in the forest soil. From the 28 P-solubilizing bacterial isolates, six isolates, named PKS037, PKS038, PKS040, PKS041, PKS043, and PKS045, could grow on the NBRIK-BTB medium and the Si-BTB medium, turning the color of the NBRIK-BTB medium from blue to yellow and generating clear rings around the colonies in the Si-BTB medium. These six isolates were screened out as PKSi-solubilizing bacteria.

To qualitatively compare the P-, K-, and Si-solubilizing activities of the six isolates, about 1 × 107 cells were grown at the center on the NBRIP-BTB, NBRIK-BTB, and Si-BTB media for 7 d and showed distinct patterns of mineral solubilization on the three media. Along the 7-d growth at the center on the NBRIP-BTB medium, the six isolates turned the color of bromothymol blue in the medium from blue to yellow from the center to the very edges of the 90-mm round NBRIP-BTB medium and generated a clear ring around the colony at the center of the medium (Fig. 1A). Apparently, the blue-to-yellow change of the bromothymol blue indicated a pH reduction from the center to the edges of the NBRIP-BTB medium and a secretion of diffusible H+ and acidic compounds into the medium from the six isolates.

Fig. 1
figure 1

Qualitative agar plate assays of bacterial phosphate (P)-, potassium (K)-, and silicon (Si)-solubilizing activities. Bacterial isolates PKS037, PKS038, PKS040, PKS041, PKS043, and PKS045 (1 × 107 colony forming units) were grown at the center of the media containing insoluble calcium phosphate (A), K-feldspar (B), and magnesium trisilicate (C) and bromothymol blue in 90-mm Petri dishes at 28 °C for 7 d. Plates without bacteria were used as control

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The six isolates grown at the center on the NBRIK-BTB medium for 7 d turned the medium color from blue to yellow but did not generate clear mineral-solubilizing zones around their colonies (Fig. 1B).

The six isolates grown at the center on the Si-BTB medium for 7 d generated clear rings around their colonies and turned the color of bromothymol blue from blue to yellow restricted in the clear rings (Fig. 1C). Magnesium trisilicate is a known antacid used to neutralize gastric acid and increase the pH of gastric juice [41] and can also be used as an adsorbent to absorb drugs, dyes and odors [42]. Magnesium trisilicate in the Si-BTB medium may restrict the diffusion of H+ and acidic compounds secreted from the Si-solubilizing bacteria and increase the pH in the clear rings via neutralization.

PKSi-solubilizing isolates reduced medium pH and dissolved insoluble minerals

The pH changes during the 7-d growth of the six isolates in the liquid NBRIP-BTB, NBRIK-BTB, and Si-BTB media were determined at 3 d and 7 d after inoculation. The pH value (7.5) of the control media without bacterial growth did not change during the 7-d period. After 3-d growth of bacteria in the liquid NBRIP-BTB, NBRIK-BTB, and Si-BTB media, the pH values of the bacterial cultures were remarkably reduced (Fig. 2A–C). During the next 4-d, the pH values of the bacterial cultures increased (PKS041, PKS040, PKS037, and PKS043) or decreased (PKS045 and PKS038) in the NBRIP-BTB medium (Fig. 2B), kept at the same levels as after 3-d growth in the NBRIK-BTB medium (Fig. 2B), and slightly increased in the Si-BTB medium (Fig. 2C). After 3-d bacterial growth, the extent of pH reduction generally showed two levels: in the NBRIP-BTB medium, the low level of pH reduction recorded as 3.0 (PKS045) and 3.3 (PKS043) while the high level recorded as 3.9 (PKS038), 4.3 (PKS037), 4.3 (PKS040) and 4.6 (PKS041) (Fig. 2A); in the NBRIK-BTB medium, the low level of pH reduction recorded as 2.7 (PKS038) and 3.2 (PKS037) while the high level recorded as 4.1 (PKS043), 4.4 (PKS045), 4.5 (PKS040), and 4.5 (PKS041) (Fig. 2B); in the Si-BTB medium, the low level of pH reduction recorded as 2.0 (PKS038) and 2.2 (PKS043) while the high level recorded as 2.9 (PKS041), 2.9 (PKS045), 3.1 (PKS037), and 3.2 (PKS040) (Fig. 2C). Generally, the extent of pH reduction was lower in the Si-BTB medium than in the NBRIP-BTB medium and the NBRIK-BTB medium; magnesium trisilicate in the Si-BTB medium worked as an antacid.

Fig. 2
figure 2

Quantitative assays of bacterial P-, K-, and Si-solubilizing activities. Bacterial isolates PKS037, PKS038, PKS040, PKS041, PKS043, and PKS045 (1 × 108 cell mL−1) were grown in liquid media (100 mL) in 250-mL Erlenmeyer flask containing insoluble calcium phosphate (A, D), K-feldspar (B, E), and magnesium trisilicate (C, F) at 180 rpm and 28 °C for 7 d. A–C pH values of the supernatant of the liquid media were measured at 3 d and 7 d after inoculation. D–F Available P (AP), available K (AK), and Available Si (ASi) in the supernatant were measured at 7 d after inoculation. Media without bacteria were used as control. Vertical bars show the standard error of mean values (n = 3). Different letters on the bars indicate significant difference between the treatments at p < 0.05

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After 7-d growth, the concentrations of AP, AK, and ASi in the bacterial cultures in the NBRIP-BTB, NBRIK-BTB, and Si-BTB media generally showed two levels (Fig. 2D–F), as the extent of the pH reduction after 3-d bacterial growth (Fig. 2A–C). In the NBRIP-BTB medium, the AP concentrations were significantly higher in PKS038, PKS037, PKS040, and PKS041 cultures (191–400 mg L−1) than in PKS045 and PKS043 cultures (70–83 mg L−1) (Fig. 2D). In the NBRIK-BTB medium, the AK concentrations were significantly higher in PKS043, PKS041, PKS040, and PKS045 cultures (10.6–12.7 mg L−1) than in PKS038 and PKS037 cultures (4.2–7.0 mg L−1) (Fig. 2E). In the Si-BTB medium, the ASi concentrations were significantly higher in PKS037, PKS041, PKS040, and PKS045 cultures (66–92 mg L−1) than in PKS038 and PKS043 cultures (41–49 mg L−1) (Fig. 2F). Seemingly, the greater the pH reduction in the NBRIP-BTB, NBRIK-BTB, and Si-BTB media, the higher the AP, AK, and ASi concentrations in the corresponding bacterial cultures, indicating that high-level bacterial release of H+ and acidic compounds led to the high level solubilization of insoluble P-, K-, and Si-minerals.

PKSi-solubilizing isolates produced and released multiple organic acids

The organic acids produced and released by the six PKSi-solubilizing isolates were determined in the supernatant from the 7-d bacterial cultures in the liquid NBRIP-BTB medium using HPLC. Among the 13 target organic acids, five organic acids (gluconic, pyruvic, propionic, succinic, and tartaric acids) were released from all the six isolates. Generally, the six isolates all released high concentrations of gluconic acid (over 1.8 mmol L−1) and low concentrations of propionic, succinic, and tartaric acids (below 0.1 mmol L−1). Five isolates released acetic, malonic, and citric acids, among which acetic acid was at high concentrations (over 1.3 mmol L−1). Four isolates released oxalic and malic acids, wherein two isolates PKS037 and PKS041 released high concentrations of oxalic acid (over 1.2 mmol L−1). Two isolates, PKS038 and PKS041, released high concentrations of lactic acid (over 0.7 mmol L−1) (Table 1).

Table 1 Organic acids released by P-, K-, and Si-solubilizing bacterial isolates in the liquid NBRIP-BTB medium after 7 d growth
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Each isolate released a distinct spectrum of organic acids (Table 1). PKS037 released oxalic, gluconic, and propionic acids at concentrations over 0.1 mmol L−1. PKS038 released gluconic, lactic, acetic, pyruvic, and malonic acids at concentrations over 0.1 mmol L−1. PKS040 released acetic and gluconic acids at concentrations over 0.1 mmol L−1. PKS041 released gluconic, acetic, oxalic, pyruvic, and lactic acids at concentrations over 0.1 mmol L−1. PKS043 and PKS045 released gluconic, acetic, and pyruvic acids at concentrations over 0.1 mmol L−1.

The sum concentrations of the target organic acids released from the six isolates in ascending order were 3.82 (PKS045), 4.67 (PKS037), 4.68 (PKS043), 5.94 (PKS040), 6.17 (PKS038), and 7.35 (PKS041) mmol L−1.

PKSi-solubilizing isolates promoted rice growth in the forest soil

The germination of the rice seeds was not interfered by the inoculation of each PKSi-solubilizing isolate. The germinated rice seedlings were sown with each of the PKSi-solubilizing isolate at an inoculation concentration of 1 × 107 CFU g−1 soil and grew for 35 d. All the six isolates promoted the growth of rice seedlings.

Comparing with the shoot height of the control seedlings without bacterial inoculation, the six isolates increased rice shoot height ranging from 11 to 25%, wherein isolate PKS041 significantly increased by 25% (Figs. 3, 4A). Comparing with the root length of the control seedlings, five isolates except PKS045 increased rice root length ranging from 38 to 72%, wherein isolate PKS037 significantly increased by 72% (Fig. 4A).

Fig. 3
figure 3

Rice seedlings grown with P-, K-, and Si-solubilizing bacterial isolates. Rice seedlings were inoculated with isolate PKS037 (a), PKS038 (b), PKS040 (c), PKS041 (d), PKS043 (e), or PKS045 (f) at 1 × 107 CFU g−1 soil and grown in the forest soil under 26 °C and a 12-h photoperiod for 35 d. Rice seedlings without bacterial inoculation were used as control

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Fig. 4
figure 4

Growth parameters of rice seedlings inoculated with P-, K-, and Si-solubilizing bacterial isolates. A Plant heights (shoot height and root length); B plant dry weight; C dry weight of shoot and root; D root-to-shoot ratio of dry weight. Rice seedlings were inoculated with isolate PKS037, PKS038, PKS040, PKS041, PKS043, or PKS045 at 1 × 107 CFU g−1 soil and grown in the forest soil under 26 °C and a 12-h photoperiod for 35 d. Rice seedlings without bacterial inoculation were used as control. Vertical bars show the standard error of mean values (n = 12). Different letters on the bars indicate significant difference between the treatments at p < 0.05

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Comparing with the dry weight of the control seedlings, the six isolates increased dry weight ranging from 26 to 163%, wherein isolates PKS037, PKS040, and PKS041 significantly increased by 76–163% (Fig. 4B); they increased shoot dry weight ranging from 20 to 143% wherein isolates PKS037, PKS040, and PKS041 significantly increased by 72–143% (Fig. 4C); they increased root dry weight ranging from 43 to 224% wherein PKS043, PKS040, and PKS041 significantly increased by 95–224% (Fig. 4C). They increased but did not significantly increase the root-to-shoot ratios of dry weight (Fig. 4D).

Grown in the forest soil contained very low levels of AP (4.9 mg kg−1), AK (34.5 mg kg−1), and ASi (23.0 mg kg−1), which are deficient for rice crops [30, 31], neither the control rice seedlings grown alone nor the rice seedlings grown with the PKSi-solubilizing bacterial isolates show visible P, K, or Si deficiency symptoms, such as dark-green leaves, chlorosis on tip of oldest leaves, or slack and droopy leaves, and seemingly had not suffered from a nutrient deficiency stress.

The dry matter concentrations of P in shoots and roots of the control rice seedlings grown alone were 0.067% and 0.054%, and in shoots and roots of the rice seedlings grown with the PKSi-solubilizing bacterial isolates were 0.066–0.083% and 0.055–0.064%, respectively (Table 2). The dry matter concentrations of K in shoots and roots of the control rice seedlings grown alone were 2.792% and 0.791%, and in shoots and roots of the rice seedlings grown with the PKSi-solubilizing bacterial isolates were 2.846–3.223% and 0.814–0.917%, respectively (Table 2). The dry matter concentrations of Si in shoots and roots of the control rice seedlings grown alone were 3.735% and 3.943%, and in shoots and roots of the rice seedlings grown with the PKSi-solubilizing bacterial isolates were 3.752–3.901% and 4.016–4.411%, respectively (Table 2). To rice seedlings, only the P contents were more likely in deficiency for rice growth and development.

Table 2 Dry matter concentrations of P, K, and Si in rice seedlings grown with P-, K-, and Si-solubilizing bacterial isolates in the forest soil
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Comparing with the P cumulative contents in the control rice seedlings, the six isolates increased P cumulative contents in rice seedlings ranging from 24 to 215%, wherein isolates PKS037, PKS038, PKS040, and PKS041 significantly increased by 84–215% (Fig. 5A); they increased P cumulative contents in rice shoots ranging from 18 to 197%, wherein isolates PKS037, PKS038, PKS040, and PKS041 significantly increased by 83–197% (Fig. 5D); they increased P cumulative contents in rice roots ranging from 45 to 280%, wherein isolates PKS043, PKS038, PKS040, and PKS041 significantly increased by 96–280% (Fig. 5D).

Fig. 5
figure 5

Phosphate (P), potassium (K), and silicon (Si) cumulative contents of rice seedlings inoculated with P-, K-, and Si-solubilizing bacteria. A–C P, K, or Si cumulative content in rice seedlings; D–F P, K, or Si cumulative content in shoots and roots of the seedlings; G–I root-to-shoot ratio of P, K, or Si cumulative content. Rice seedlings were inoculated with isolate PKS037, PKS038, PKS040, PKS041, PKS043, or PKS045 at 1 × 107 CFU g−1 soil and grown in the forest soil for 35 d. Rice seedlings without bacterial inoculation were used as control. Vertical bars show the standard error of mean values (n = 12). Different letters on the bars indicate significant difference between the treatments at p < 0.05

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Comparing with the K cumulative content in the control rice seedlings, the six isolates increased K cumulative contents in rice seedlings ranging from 36 to 170%, wherein isolates PKS037, PKS040, and PKS041 significantly increased by 76–170% (Fig. 5B); they increased K cumulative contents in rice shoots ranging from 33 to 163%, wherein isolates PKS037, PKS040, and PKS041 significantly increased by 74–163% (Fig. 5E); they increased K cumulative contents in rice roots ranging from 66 to 253%, wherein isolates PKS043, PKS040, and PKS041 significantly increased by 117–253% (Fig. 5E).

Comparing with the Si cumulative contents in the control rice shoots, the six isolates increased Si cumulative contents in rice seedlings ranging from 24 to 177%, wherein isolates PKS037, PKS040 and PKS041 significantly increased by 81–177% (Fig. 5C); they increased Si cumulative contents in rice shoots ranging from 18 to 149%, wherein isolates PKS040, PKS037 and PKS041 significantly increased by 72–149% (Fig. 5F); they increased Si cumulative contents in rice roots ranging from 45 to 260%, wherein isolates PKS043, PKS037, PKS040, and PKS041 significantly increased by 97 ‒ 260% (Fig. 5F).

The six isolates increased the root-to-shoot ratios of P, K, and Si cumulative contents (Fig. 5G–I) wherein only isolate PKS041 significantly increased the root-to-shoot ratio of Si cumulative content (Fig. 5I).

After 35-d growth of rice seedlings, the pH value of the non-inoculation control soil was 5.17 while the pH values of the inoculated soil were 5.10–5.14. PKSi-solubilizing isolates and rice seedlings slightly increased AP in the soil comparing with AP in the non-inoculation control soil (Fig. 6A). PKSi-solubilizing isolates and rice seedlings reduced AK in the soil, wherein isolate PKS038 and rice seedlings significantly reduced AK in the soil comparing with AK in the non-inoculation control soil (Fig. 6B). PKSi-solubilizing isolates and rice seedlings significantly increased ASi in the soil comparing with ASi in the non-inoculation control soil (Fig. 6C).

Fig. 6
figure 6

Available phosphorus (AP), available potassium (AK), and available silicon (ASi) concentrations in the forest soil grown with rice seedlings and P-, K-, and Si-solubilizing bacteria. Rice seedlings were inoculated with isolate PKS037, PKS038, PKS040, PKS041, PKS043, or PKS045 at 1 × 107 CFU g−1 soil and grown in the forest soil for 35 d. Rice seedlings without bacterial inoculation were used as control. Vertical bars show the standard error of mean values (n = 12). Different letters on the bars indicate significant difference between the treatments at p < 0.05

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Generally, isolates PKS041, PKS040, and PKS037 significantly increased dry weight, P, K, and Si cumulative contents of rice seedlings, while isolate PKS041 increased them more significantly than other isolates.

Six PKSi-solubilizing isolates belong to five proteobacteria genera

The six PKSi-solubilizing isolates were classified to genus level based on their rrs sequence similarities and phylogenetic relationships to the type strains of closely related species. Isolate PKS037 was classified into genus Pseudomonas within class Gammaproteobacteria; isolate PKS038 was classified into genus Agrobacterium within class Alphaproteobacteria; isolates PKS040, PKS041, PKS043, and PKS045 were classified into genus Collimonas, Burkholderia, Paraburkholderia, and Paraburkholderia within class Betaproteobacteria, respectively.

The amplified partial rrs sequences of the six isolates are deposited at the GenBank database under the accession numbers OR731511–OR731516. The rrs sequence of isolate PKS037 (1414 bp) shows similarity > 98.65% (the threshold for differentiating two species) [43] to over 50 genomospecies within genus Pseudomonas and the closest phylogenetic relationship to P. atagonensis, P. glycinae, P. fitomaticsae, and P. kribbensis (Fig. 7) within the Pseudomonas koreensis subgroup [44] of the Pseudomonas fluorescens complex [45]. The rrs sequence of isolate PKS038 (1407 bp) is identical to the corresponding sequences of Agrobacterium tumefaciens and A. arsenijevicii. The rrs sequence of isolate PKS040 (1415 bp) shows similarity > 98.65% to five genomospecies within genus Collimonas and the closest phylogenetic relationship to Collimonas sp. Ter331 and C. fungivorans Ter6 (Fig. 7). The rrs sequence of isolate PKS041 (1422 bp) shows similarity > 98.65% to 31 genomospecies within the genus Burkholderia and the closest phylogenetic relationship to Burkholderia stagnalis, B. stabilis, B. pyrrocinia, and Burkholderia sp. EB159 (Fig. 7). The rrs sequence of isolate PKS043 (1410 bp) shows similarity of 99.93% and the closest phylogenetic relationship to Paraburkholderia caffeinilytica (Fig. 7). The rrs sequence of isolate PKS045 (1420 bp) shows similarity > 98.65% to six genomospecies within genus Paraburkholderia and the closest phylogenetic relationship to Paraburkholderia elongata (Fig. 7).

Fig. 7
figure 7

Phylogenetic tree showing bacterial phylogeny and taxonomy status of the P-, K-, and Si-solubilizing isolates PKS037, PKS038, PKS040, PKS041, PKS043, and PKS045 based on 16S rRNA gene sequences (1345 positions). The 16S rRNA gene sequences of the type strains or representative strains of closely related species were extracted from EzBioCloud (https://www.ezbiocloud.net). All positions containing gaps and missing data were eliminated. Sequence accession numbers are indicated after the strain names. The phylogenetic tree was generated using the maximum likelihood method based on the Tamura–Nei model using MEGA5. A discrete Gamma distribution was used to model evolutionary rate differences among sites. Bootstrap values (> 50%) of 1000 tests are shown at the nodes. The scale bar indicates 0.01 substitutions per site

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Discussion

Forest soil is a resource of PKSi-solubilizing bacteria for crop production

We screened out six PKSi-solubilizing bacterial isolates from the forest soil with low AP, AK, and ASi and demonstrated their capability of mobilizing soil insoluble P, K, and Si minerals and supplying soil P, K, and Si to rice plants. The six PKSi-solubilizing isolates promoted the growth of rice seedlings in the forest soil by increasing soil AP and ASi, plant P, K, and Si cumulative contents and dry weight, and the root-to-shoot ratio of P, K, and Si cumulative contents and dry weight.

We initiated the screening using the widely used NBRIP-BTB medium to select P-solubilizing bacteria [36]. Our initial selection focused on the mineral-solubilizing bacteria abundant in the target forest soil. From the isolates at an abundance higher than 1 × 107 CFU g−1 soil, 83% (45 of 54) isolates reduced the pH around their colonies on the NBRIP-BTB medium and 52% (28 of 54) isolates showed clear P-solubilizing activity in association with reducing the medium pH. The NBRIP-BTB medium effectively selected P-solubilizing bacteria abundant in the low-AP forest soil.

From the 28 P-solubilizing isolates, six isolates showed clear Si-solubilizing activity on the Si-BTB medium containing simply glucose and magnesium trisilicate [34]. The glucose in the NBRIP-BTB and Si-BTB media likely stimulates bacterial production of low-molecular-weight organic acids, particularly gluconic acid, leading to the reduction of medium pH and acidification-mediated mineral solubilization. The periplasmic oxidation of glucose by the membrane bound glucose dehydrogenase and the cofactor pyrroloquinoline quinone is probably the most cost-efficient microbial pathway to produce organic acids and lead to external acidification and mineral solubilization [46, 47]. The silicate source magnesium trisilicate in the Si-BTB medium also showed its antacid activity via restricting the diffusion of H+ and organic acids in the solid medium around the Si-solubilizing bacterial colonies and retarding the pH reduction in the liquid bacterial culture.

The P-solubilizing isolates reduced the pH in the NBRIK-BTB medium but did not generate a clear K-solubilizing ring around their colonies. The pH reduction and weak K-solubilizing activity were certified from the liquid cultures of the six PKSi-solubilizing isolates. Seemingly, the NBRIK-BTB medium derived from the NBRIP-BTB medium is not efficient for qualitative screening of K-solubilizing bacteria; the K source, K-feldspar, in the NBRIK-BTB medium may be difficult to dissolve.

The six PKSi-solubilizing isolates show limited diversity but representative taxa of mineral-weathering bacteria. First, the NBRIP-BTB medium, which effectively selects the acidification-mediated P-solubilizing bacteria, initially limited the bacterial diversity. The most frequent and effective K-solubilizing bacteria and Si-solubilizing bacteria belonging to the genus Bacillus [11, 13,14,15,16] were not present among the initial 28 P-solubilizing isolates. Second, our attention on the PKSi-solubilizing bacteria at high abundance in the target forest soil further limited the bacterial diversity. However, the six PKSi-solubilizing isolates belonging to the genera Burkholderia, Paraburkholderia, and Collimonas (within class Betaproteobacteria), Pseudomonas (within class Gammaproteobacteria), and Agrobacterium (within class Alphaproteobacteria) represent the common mineral-weathering bacterial taxa, indicating that this small-scale initial screening is effective. Bacteria within the genera Burkholderia [48, 49], Paraburkholderia [50,51,52,53], and Collimonas [49, 54, 55] are common mineral-weathering bacteria in both deciduous and coniferous forest soils. Likewise, bacteria within the Pseudomonas fluorescens complex [24, 56] and the genus Agrobacterium [57, 58] are common mineral-weathering bacteria in soils.

Acidification in association with organic acids determines P, K, and Si solubilization

The six PKSi-solubilizing isolates showed diverse P-, K-, or Si-solubilizing activities and produced diverse organic acids. Generally, the levels of their mineral-solubilizing activities were positively correlated with the level of pH reduction in the medium and the level of gluconic acid released into the medium. In contrast to the similar pH reduction of 4.3 and 3.9 in the respective liquid NBRIP-BTB culture of isolate PKS037 and isolate PKS038 after 3-d growth and the similar AP concentration in the culture of isolate PKS037 (214 mg L−1) and isolate PKS038 (191 mg L−1) after 7-d growth, the sum concentration of the organic acids released from the isolate PKS037 (4.67 mmol L−1) was remarkably lower than that from the isolate PKS038 (6.17 mmol L−1). A speculation is that oxalic acid at high concentration (1.89 mmol L−1) released from the isolate PKS037 substantially contributed to the pH reduction and P-solubilization, whereas lactic acid (1.63 mmol L−1) and acetic acid (1.47 mmol L−1) at high concentration released from the isolate PKS038 did not. In line with this speculation, oxalic acid is one of the most common low-molecular-weight organic acids found in soils [59, 60] and secreted by microbial communities in soils [61], mediating mineral weathering in soils [59,60,61,62].

The pH values of the cultures of the six isolates in the liquid Si-BTB medium and the cultures of the four isolates PKS041, PKS040, PKS037, and PKS043 in the liquid NBRIP-BTB medium increased after 3-d growth. The cause of the pH increase in the two media may be different. The general pH increase in the Si-BTB medium may be the result of the antacid activity of magnesium trisilicate. In the liquid NBRIP-BTB medium, acidification-mediated high-level P-solubilization provides AP for high-level bacterial growth, resulting in the pH increase after exhaustion of glucose and consumption of organic acids, as Srinivasan and Mahadevan suggested [63].

Microbe–soil–plant interactions determine P, K, and Si solubilization and plant growth promotion

To test their potential to mobilize soil P, K, and Si for crop nutrition, the PKSi-solubilizing strains were individually inoculated to the air-dried but non-sterilized forest soil and the model crop rice. First, the PKSi-solubilizing bacterial isolates are indigenously high abundant and adapted to the acidic forest soil with low AP, AK, and ASi. Second, the high-performance PKSi-solubilizing bacteria screened out should be competitive among the indigenous microbiome. Third, the low AP, AK, and ASi status likely induces the bacterial PKSi-solubilizing activities. Fourth, the rice crop prefers to grow in slightly acidic soils. Fifth, the rice crop in the subtropical regions in China frequently faces the soil acidification problem.

The rice seedlings grown alone and with a PKSi-solubilizing bacterial strain in the forest soil with deficient AP, AK, and ASi for rice crops for 35 d did not show visible nutrient deficiency symptoms [64] and seemingly had not suffered from a nutrient deficiency stress. However, the dry matter concentrations of P in the seedlings (0.06–0.08%) indicate the P contents were deficient [64, 65]. The P deficiency seemingly did not seriously limit the growth of the rice seedlings but may limit their further development, such as tillering.

The six PKSi-solubilizing strains showed their P-, K-, and Si-solubilizing activities in the forest soil and increased rice uptake of P, K, and Si, thus mitigating the possible nutrient deficiency. In contrast to the increase of AP and ASi in the forest soil, the commensalism of a PKSi-solubilizing strain and rice seedlings in the forest soil reduced the soil AK. Likely, the six PKSi-solubilizing strains have relatively weak K-solubilizing activities in the NBRIK-BTB medium and the forest soil comparing with their P- and Si-solubilizing activities. However, they supported the rice seedlings with high K use efficiency and uptake from the forest soil, resulting in no K deficiency in the rice seedlings. Notably, the increases of the P, K, and Si cumulative contents in roots and shoots are in line with the increases of the corresponding dry weights of roots and shoots, and the increases of their root-to-shoot ratios. More likely, the increased P, K, and Si contents support the increased biomass. Therefore, the PKSi-solubilizing activity is the key factor for the plant growth-promotion.

The paddy rice generally adapts to low pH [66]. Here, the control rice seedlings grown alone in the acidic forest soil (pH 4.95) without bacterial inoculation for 35 d did not show visible decline or damage in leaves and roots and did not reduce the soil pH but increased 0.22. This pH change may be the result of the acidification associated with the uptake of NH4+ and the alkalization associated with the uptake of NO3− from the soil by the rice seedlings [66] and the secretion of organic acids by rice roots response to nutrient deficiency [67]. The rice seedlings grown with the inoculated PKSi-solubilizing strains did not reduce the soil pH but increased 0.15–0.19. This pH change may be the complex result of the rice seedling uptake of NH4+ and NO3− from the soil, response to nutrient deficiency and the mitigation of nutrient deficiency by the PKSi-solubilizing strains. Particularly, the PKSi-solubilizing strains significantly increased the soil ASi. The enhanced Si supply and uptake may reduce rice root secretion of organic acids, retarding the rhizosphere acidification [68]. The enhanced Si supply and uptake may also increase P solubility and uptake by competing with the adsorption sites in cell walls with P [68] and upregulated P transporters in roots [69, 70].

Conclusion

The forest soil with low available P, K, and Si is a valuable resource for high-performance PKSi-solubilizing bacteria improving soil fertility and crop nutrition. The result of this small-scale pilot screening of high-performance PKSi-solubilizing bacteria is encouraging. The NBRIP-BTB and Si-BTB media effectively selected acidification-directed P- and Si-solubilizing bacteria. Six PKSi-solubilizing strains representative of common mineral-weathering bacterial taxa were successfully screened out and promoted the growth of rice seedlings by solubilization of P, K, Si and mobilization of P, K, and Si to plants in the acidic soil with low available P, K, and Si. The PKSi-solubilizing strains show the potential to mitigate soil P, K, and Si deficiency and promote crop growth. They may recover soluble P, K, and Si from chemical fertilizers and improve the use efficiency of chemical fertilizers, thus reducing the input of chemical fertilizers. They may retard soil acidification by Si-solubilization and improve soil quality. They will be further scrutinized on their field application potential of improving soil fertility and crop production and the possible neutralization of soil acidification by Si-solubilization.

Availability of data and materials

No datasets were generated or analyzed during the current study.

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Funding

This work was supported by the Fundamental Research Funds for the Central Universities (226-2023-00077, 226-2024-00052), the National Key Research and Development Program of China (2018YFD0800202), the National Key Research and Development Program of Ningbo (2022Z175), the National Natural Science Foundation of China (32201916), and the Guangxi Provincial Natural Science Foundation of China (2021GXNSFDA196004).

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Authors and Affiliations

  1. Ministry of Education Key Laboratory of Environment Remediation and Ecological Health, College of Environmental & Resource Sciences, Zhejiang University, Hangzhou, 310058, China

    Lei Zhang, Che Tan, Wenjuan Li, Xiaoping Fan, Hongyun Peng & Yongchao Liang

  2. Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture and Rural Affairs, Guangxi Key Laboratory of Sugarcane Genetic Improvement, Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, Nanning, 530007, China

    Li Lin

  3. State Key Laboratory of Rice Biology and Breeding, Key Laboratory of Molecular Biology of Crop Pathogens and Insects Ministry of Agriculture and Rural Affairs, Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Biotechnology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China

    Tianlan Liao & Qianli An

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  1. Lei Zhang
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  2. Che Tan
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  3. Wenjuan Li
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  4. Li Lin
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  9. Yongchao Liang
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Contributions

LZ: investigation, methodology, formal analysis, visualization, writing—original draft. CT: investigation, methodology, and formal analysis. WL: investigation. LL: conceptualization, methodology, funding acquisition, and project administration. TL: investigation. XF: methodology and resources. HP: methodology, resources and project administration. AQ: conceptualization, visualization, funding acquisition, supervision, and writing—original draft. YL: conceptualization, funding acquisition, supervision, and writing—review and editing. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Li Lin, Qianli An or Yongchao Liang.

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Zhang, L., Tan, C., Li, W. et al. Phosphorus-, potassium-, and silicon-solubilizing bacteria from forest soils can mobilize soil minerals to promote the growth of rice (Oryza sativa L.). Chem. Biol. Technol. Agric. 11, 103 (2024). https://doi.org/10.1186/s40538-024-00622-9

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