DOI: https://doi.org/10.56669/YTAX1606
ABSTRACT
Phosphorus (P) is an essential plant macronutrient; however, less than 1% of the total P content in global soils is available to plants due to widespread P fixation, wherein 75% to 90% of applied soluble inorganic fertilizers rapidly form insoluble complexes, often referred to as legacy P. This necessitates sustainable alternatives, given the energy-intensive nature of chemical fertilizer synthesis, the non-renewable status of phosphate rock, and the environmental risk of water eutrophication. Phosphate-solubilizing bacteria (PSB) offer an eco-friendly and biologically efficient strategy to enhance P utilization. P mobilization by PSB fundamentally relies on two pathways: mineral P solubilization and organic P mineralization. Solubilization of mineral P (e.g., tricalcium phosphate) is achieved primarily through the secretion of low-molecular-weight organic acids (such as gluconic acid). These acids chelate cations or release H+ ions, lowering the surrounding pH and converting fixed P into forms accessible to plants. Organic P is mineralized through the action of PSB-secreted enzymes, particularly phosphatases (acid, alkaline, and neutral) and phytases, which hydrolyze organic compounds to release orthophosphate. The genetic potential for these mechanisms is widespread, encompassing genes such as pqqE for acid secretion and phoD for alkaline phosphatase production. Beyond P mobilization, PSB strains are often multifunctional, promoting plant growth by producing phytohormones such as indole-3-acetic acid and 1-aminocyclopropane-1-carboxylate deaminase, and by producing siderophores. PSB are a vital component of integrated plant nutrient management systems. They exhibit synergistic effects when co-applied with sparingly soluble phosphate rock, organic amendments, or in multi-specific consortia alongside other PSB strains, arbuscular mycorrhizal fungi, or N-fixing bacteria. In Taiwan, PSB products constitute the predominant category of registered microbial fertilizers. The commercialized strains are mainly from the Bacillus genus, with B. subtilis, B. amyloliquefaciens, and B. safensis collectively representing 76% of registered products. Continued government support aims to advance the microbial fertilizer industry and reduce reliance on chemical inputs.
Keywords: phosphate-solubilizing bacteria, legacy P, organic acids, plant growth promotion, commercialization
INTRODUCTION
Phosphorus (P) is an essential plant macronutrient, ranking second in importance after nitrogen (N), and plays a crucial role in regulating agricultural production (Akplo et al., 2025). P is indispensable for plant development, involved in core metabolic processes such as cell division, energy production (ATP), macromolecule synthesis, signal transduction, and photosynthesis (Zhong et al., 2023).
Despite the relatively high total P content in global soils, generally ranging from 50–3000 mg kg-1, only a negligible amount (<1%) is available to plants (Richardson et al., 2009; Akplo et al., 2025). The primary challenge arises from the widespread phenomenon of P fixation or immobilization, in which 75% to 90% of applied soluble inorganic fertilizers rapidly bind to metal cations (Ca, Al, Fe), forming insoluble complexes that plants cannot utilize (Sharma et al., 2013). This accumulated, fixed P is often referred to as legacy P (Némery and Garnier, 2016; Li et al., 2023).
The necessity for sustainable alternatives is driven by multiple factors, including the highly energy-intensive processes involved in chemical fertilizer synthesis, the non-renewable nature of phosphate rock resources, and the environmental risks associated with excessive P runoff, particularly water eutrophication (Mueller et al., 2012; Sharma et al., 2013). Phosphate-solubilizing microorganisms (PSM) offer an eco-friendly, low-cost, and biologically efficient strategy to enhance P utilization efficiency in sustainable cropping systems (Timofeeva et al., 2022).
PHYLOGENETIC AND ECOLOGICAL DISTRIBUTION OF PSB
Among the whole microbial population in soil, phosphate-solubilizing bacteria (PSB) comprise 1–50% and phosphate-solubilizing fungi (PSF) 0.1 to 0.5% of the total respective population (Kalayu, 2019). According to recent studies, the currently known PSB strains are generally members of three phyla: Actinomycetota (Actinobacteria), Bacillota (Firmicutes), and Pseudomonadota (Proteobacteria). At the genus level, PSB strains have been classified within the genera Acinetobacter, Aeromonas, Agrobacterium, Alcaligenes, Arthrobacter, Azotobacter, Bacillus, Bradyrhizobium, Burkholderia, Citrobacter, Cyanobacteria, Delftia, Enterobacter, Erwinia, Gordonia, Klebsiella, Kushneria, Micrococcus, Paenibacillus, Pantoea, Phyllobacterium, Pseudomonas, Rhizobium, Rhodococcus, Salmonella, Serratia, Sinomonas, Sphingobium, Streptomyces, Thiobacillus, and Xanthomonas (Timofeeva et al., 2022; Li et al., 2023).
The ecological niches of PSB encompass diverse habitats, including general soil environments; the rhizospheres of corn, rice, wheat, cowpea, grass, oil palm, spiny deciduous shrub, and giant cardon cactus; lateritic soils; acid sulfate soils; calcareous soils; tropical and subtropical soils; mangrove ecosystems; wheat grains; as well as P-rich substrates such as Indian rock phosphate and Venezuelan phosphate rocks (Song et al., 2022; Timofeeva et al., 2022).
MECHANISMS OF PHOSPHATE MOBILIZATION
P mobilization is fundamentally achieved through mineral P solubilization and organic P mineralization, and the physiological and molecular mechanisms involved are summarized below.
Mineral P solubilization
Physiological mechanisms
Mineral P sources such as tricalcium phosphate (Ca3(PO4)2), aluminum phosphate (AlPO4), and iron phosphate (FePO4) can be utilized by solubilizing action of acids and chelation. It is widely recognized that PSB secrete low-molecular-weight organic acids, which chelate cations bound to phosphate via their hydroxyl and carboxyl groups, or release H+ ions that lower the surrounding pH (Chen et al., 2006; Lin et al., 2006; Li et al., 2023). These processes convert fixed P into a form that plants can readily access. The predominant organic acids produced by PSB and involved in P-solubilization include acetic acid, ascorbic acid, butyric acid, citric acid, formic acid, gluconic acid, isobutyric acid, isovaleric acid, 2-ketogluconic acid, lactic acid, malic acid, oxalic acid, oxyglutaric acid, propanedioic acid, propionic acid, pyruvic acid, succinic acid, and tartaric acid (Li et al., 2023).
Molecular mechanisms
Many genes involved in acid secretion that enhance the solubilization of mineral P through genetic manipulation have been studied (Li et al., 2023). Researchers cloned the Erwinia herbicola pyrroloquinoline quinone (PQQ) synthase gene into Escherichia coli HB101, enabling the bacteria to synthesize PQQ (Liu et al., 1992). This cofactor activates glucose dehydrogenase, enabling Escherichia coli to convert glucose into gluconic acid, thereby increasing acid secretion and improving the solubility of mineral P. Amino acid sequence alignment data from several bacterial species showed that the pqqE gene is highly conserved and is a hallmark gene in hydroxyapatite solubilization (Ludueña et al., 2016). Introducing the 396-base gabY gene from Pseudomonas cepacia into Escherichia coli JM109 was enough to trigger the mineral P solubilization and gluconic acid production (Babu-Khan et al., 1995). Although gabY does not resemble known direct-oxidation pathway genes, its predicted protein shares substantial sequence similarity with membrane proteins of the histidine permease (HisQ) family. In addition, a DNA fragment from Serratia marcescens was shown to induce gluconic acid synthesis in Escherichia coli DH5α, but it does not exhibit any homology to the previously characterized genes (Krishnaraj and Goldstein, 2001).
Organic P mineralization
Physiological mechanisms
Organic matter represents the second major pool of soil P, with organic P generally comprising 30–50% of total soil P. Most organic P is found as inositol phosphate (phytate), while additional forms include phosphomonoesters, phosphodiesters including phospholipids and nucleic acids, and phosphotriesters (Rodríguez and Fraga, 1999). The mineralization of organic P by enzymes secreted by PSB represents a major dephosphorylation pathway, primarily mediated by phosphatase, phytases, and C-P-cleaving enzymes (Pan and Cai, 2023). Phosphatases are classified as acidic, alkaline, or neutral. Acid phosphatases are most effective in mineralizing organic P in acidic soils, whereas alkaline phosphatases primarily hydrolyze phospholipids and release orthophosphate in alkaline soils. Neutral phosphatases exhibit comparatively limited activity in P mineralization. Phytase mineralizes phytate-bound organic P, producing intermediates that phosphatases can further hydrolyze to release orthophosphate, since phytate’s ester bonds are otherwise too stable to break (Pan and Cai, 2023).
Molecular mechanisms
Many of the genes in PSB encode different enzymes, such as alkaline phosphatases (phoA, phoD, phoX), acid phosphatases (phoC), phytase (appA), C-P cleavage enzyme (phn), extracellular polyphosphatase (ppx), and polyphosphate kinase (ppk), with alkaline phosphatases being the most studied (Pan and Cai, 2023). Under inorganic P limitation, bacteria activate the P starvation (Pho) regulon and induce alkaline phosphatase production, enabling energy-efficient enzyme synthesis and switching P uptake to an alternative transport system (Vershinina and Znamenskaya, 2002). Three homologous genes—phoA, phoD, and phoX—associated with alkaline phosphatase production have been identified within the Pho regulon, and 31.9% of 3,058 sequenced prokaryotic genomes possess at least one of these genes, indicating broad genetic potential for alkaline phosphatase synthesis (Zimmerman et al., 2013). In soil bacteria, phoD was the most frequently detected alkaline phosphatase gene in 16S rRNA-associated metagenomic datasets, with phoA and phoX also detected (Tan et al., 2013). Although phoA was initially thought to be the primary source of alkaline phosphatase in marine ecosystems, more recent findings indicate that phoX is more widely distributed among marine bacteria and is induced exclusively under P starvation (Sebastian and Ammerman, 2009). PafA is a phosphate-insensitive phosphatase widely distributed in Bacteroidota (Bacteroidetes) and abundant in natural environments, where it plays a major role in regenerating phosphate (Lidbury et al., 2022). The pafA gene is highly diverse in plant rhizospheres, and it is abundant in the global ocean, where it is expressed independently of P availability.
ADVANCES AND CHALLENGES IN SCREENING AND FORMULATION OF PSB
The key developments in screening potential PSB are outlined, and the remaining challenges in inoculant formulation and quality control are highlighted.
Optimization of liquid medium formulation
Historically, PSB isolation relied on the halo/zone assay on Pikovskaya solid medium (PVK) (Pikovskaya, 1948). Later, a newly formulated medium, the National Botanical Research Institute’s phosphate growth medium (NBRIP), was adopted, which enabled the detection of about 3-fold higher phosphate-solubilizing activity in broth assay compared to PVK (Nautiyal, 1999). Using this improved formulation for phosphate solubilization assays, it demonstrated that many bacterial strains that did not form a visible halo/zone on agar plates could still exhibit measurable phosphate-solubilizing activity in liquid medium. Therefore, the NBRIP broth assay provides a more effective approach for screening for the most efficient PSB.
Rapid visual test for PSB
An efficient visual method was established for the qualitative screening of PSB (Mehta and Nautiyal, 2001). The incorporation of bromophenol blue allows for rapid qualitative detection of strains capable of solubilizing P. The formulation can also be used as a quality control test to expeditiously screen commercial bioinoculant preparations based on P solubilizers.
Guidelines used for isolating and testing PSB
Reviews of the literature and chemical considerations related to phosphate solubilization by microorganisms have shown that the commonly used selection factor for this trait, tricalcium phosphate (Chen et al., 2006), is relatively weak and unreliable as a universal selection factor for isolating and testing PSB for enhancing plant growth (Bashan et al., 2013a). Consequently, Bashan et al. (2013b) proposed a set of guidelines for identifying PSB with real agronomic potential, providing a more reliable framework for their evaluation. These guidelines are summarized below.
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A combination of two or three metal-P compounds, when used together or in tandem, should replace the sole tricalcium as an initial selection factor. The selection of metal-P candidates for potential PSB will depend on the soil type where the PSB will be used. Adding other Ca-P compounds, such as rock phosphates for alkaline soils, Al-P and Fe-P compounds for acidic soils, is suggested.
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The few bacterial isolates that are positive in both the halo/zone assay and broth assay should be further tested for abundant production of organic acids.
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Isolates complying with the above criteria should be tested on a model plant as the ultimate test for potential P solubilization. Parameters related to P nutrition in plants should be tested, not growth promotion in general, because growth promotion can result from other mechanisms.
Inoculant formulation
The transfer from laboratory efficacy to commercial success requires a robust inoculant formulation. Inoculant carriers can be divided into five basic categories: (1) Soils: peat, coal, clays, and inorganic soil, (2) Waste plant materials of diverse agriculture origins: lignin, soybean or wheat bran, grape bagasse and banana waste, (3) Inert materials: polymers, treated rock fragments such as vermiculite and perlite, (4) Plain lyophilized microbial cultures and oil-dried bacteria that can later be incorporated into a solid carrier or used as they are, and (5) Liquid inoculants, where chemicals such as carboxymethyl cellulose, glycerol, trehalose, gum Arabic, were added to the liquid medium to improve stickiness, stabilization, surfactant, function, and dispersal (Bashan et al., 2014). Although no ideal formulation exists and each type presents distinct strengths and limitations, certain key steps in inoculant production require careful attention (Herrmann and Lesueur, 2013). Choices made during these steps ultimately dictate the success or failure of inoculation. Regardless of the specific formulation, the final inoculant can be of four types: liquid, slurry, granular, or powder. Any formulation must be stable during production, distribution, storage, and transportation to the farmer, particularly when the main ingredient is alive and susceptible to changes.
Quality control
Many inoculants currently available in the market are of poor quality, leading to a loss of confidence among farmers. Practical methods for the quality control of inoculant biofertilizers have been proposed by the Australian Centre for International Agricultural Research (ACIAR) (Deaker et al., 2011). Quality control should verify that there are sufficient viable numbers of the correct strains of microorganisms in the biofertilizer throughout the product's shelf life. Farm trials should also be part of quality control, demonstrating that the biofertilizer actually increases crop yield while reducing chemical fertilizer inputs. A high-quality inoculant must satisfy both farmers and producers by containing a large number of one or more strains that deliver maximal, consistent, and reproducible performance across varying field environments; remaining free from major contaminants and opportunistic pathogens affecting humans, animals, or plants; and maintaining an extended shelf life capable of tolerating typical on-farm handling (Herrmann and Lesueur, 2013).
MULTIFUNCTIONALITY AND GROWTH-PROMOTING POTENTIAL OF PSB
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Plant growth-promoting traits
Beyond P solubilization, PSB often possess the ability to modify root functioning to enhance P acquisition through bacterial plant growth-promoting activities (Bargaz et al., 2021; Chen et al., 2021).
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Phytohormone production: PSB inoculation can increase the germination percentage of seeds by secreting indole-3-acetic acid (IAA), hence playing a major role in the regulation of endogenous IAA level with positive consequences on P acquisition and plant physiological status (Song et al., 2022).
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1-aminocyclopropane-1-carboxylate (ACC) deaminase activity: The root length and root biomass of rice plants strongly correlated with ACC deaminase produced by Alcaligenes sp. with P-solubilizing trait, and led to improved shoot growth (Bal et al., 2013).
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Nitrogen fixation: The main advantage of PSB with N-fixing activity is their beneficial nutritional effect resulting from both P mobilization and N fixation (Peix et al., 2001).
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Siderophore production: PSB can mobilize Fe–P via siderophore production, thereby facilitating the conversion of insoluble P and Fe into more available forms (Cui et al., 2022).
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PSB as a biofertilizer for diverse crop species
As a member of plant growth-promoting rhizobacteria, PSB can promote plant growth through a wide range of mechanisms, and its agricultural potential continues to increase as it provides an appealing alternative to chemical fertilizers. For example, inoculation with the two auxin-producing PSB increased both P concentration and auxin levels in wheat plants, resulting in greater plant biomass (Kudoyarova et al., 2017). This highlights the importance of elevated auxin content in stimulating root growth and enhancing P uptake capacity in response to PSB. The P-solubilizing and IAA-producing Paenibacillus sp. B1 significantly increased maize root and shoot length, enhanced phosphorus and nitrogen uptake, and raised total dry biomass (Li et al., 2017). The growth-promoting effects of PSB have been demonstrated across a broad range of crop categories, including cereals (wheat, maize, sorghum, rice, barley), legumes (peanut, soybean, beans, chickpea), oilseed crops (canola), root and tuber crops (potato, radish, sugar beet), vegetables (lettuce, tomato), fruit crops (apple, citrus), industrial crops (sugarcane), and various ornamental plants (Kalayu, 2019).
AGRONOMIC INTEGRATION AND COMPLEX MICROBIAL INTERACTIONS
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Integrated nutrient management and legacy P utilization
PSB serve as a vital component in an integrated plant nutrient management system (IPNMS), maximizing the efficiency of applied and native P sources (Bargaz et al., 2018). The combined use of microbial and mineral resources is an emerging research area that aims to develop efficient microbial formulations compatible with mineral inputs, with positive effects on both crops and the environment.
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Synergy with P fertilizers: Microbial-based bioformulations that increase plant performance and exhibit complementary and synergistic effects with mineral fertilization are greatly needed (Bargaz et al., 2018). Co-applications of elite PSB strains with sparingly soluble rock phosphate or tricalcium phosphate have been demonstrated to increase available P content in the soil as well as plant P uptake and plant biomass in the pot experiment and field trial (Kaur and Reddy, 2015; Zineb et al., 2020; Song et al., 2022).
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Organic amendments: PSB synergize effectively with organic amendments such as cow dung manure, which improved P content and growth of Brassica juncea (Singh et al., 2014). The combined application of bio-organic phosphate and the PSB significantly enhanced the growth, yield parameters, and productivity of two wheat cultivars compared to non-inoculated control treatments (Tahir et al., 2018). A study demonstrated that partial replacement of mineral P with organic manure could reshape the phosphate-solubilizing and alkaline phosphomonoesterase-producing bacterial communities, making them more resilient and effective for high P utilization and productivity under intensive cultivation (Bi et al., 2020).
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Legacy P activation: Global agricultural soils contain enough accumulated P to support crop production for roughly a century. Consequently, researchers have explored the potential of soil “P activators” to mobilize this legacy P for plant use (Zhu et al., 2018; Li et al., 2023). Although results have varied, growing evidence indicates that these activators can increase soil phosphate availability and help alleviate the global P crisis.
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Microbial consortia and multi-species interactions
Single-strain inoculation often yields inconsistent field results due to competition and environmental variability. Using multi-specific consortia is generally considered a more robust approach (Zineb et al., 2020).
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PSB consortia: The pot experiment illustrated that available P in the soil, as well as plant P uptake, could be improved with inoculation of a mixture of PSB (Song et al., 2022). Inoculating plants with P-efficient bacterial consortia is an emerging research area that requires attention to identify microbial combinations that can enhance both above- and below-ground performance, thereby increasing plant growth and yield (Bargaz et al., 2021).
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PSB and Arbuscular mycorrhizal fungi (AMF): In a study on the interactions between PSB and AMF, it was found that AMF affected the growth of different PSB strains, and the other bacterial strains also had substantial effects on the development of AMF extraradical hyphae outside carrot roots and on the colonization of potato roots by AMF (Ordoñez et al., 2016). Dual inoculation with PSB and AMF enhanced plant biomass and nutrient (N and P) accumulation, likely because PSB released phosphate that AMF efficiently absorbed (Toro et al., 1997). These interactions between bacteria and fungi supported P cycling and provided a more sustainable nutrient supply for plants. A synergetic effect of PSB, AMF, and phosphor-compost was demonstrated in tomato seedlings, which showed enhancement in P solubilization and plant growth (El Maaloum et al., 2020).
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PSB and diazotrophs: Co-inoculation of PSB and mixed rhizobial culture significantly enhanced the plant growth, shoot P and N concentrations, nodulation efficiency, and nitrogenase activity (Gull et al., 2004). Dual inoculation with PSB (Pseudomonas) and N-fixing bacteria (Bradyrhizobium) significantly enhanced symbiotic nitrogen fixation, nutrient acquisition, and soybean growth in pot and field experiments (Tu et al., 2021; Kumawat et al., 2022).
LIMITATIONS IN THE AGRICULTURAL APPLICATION OF PSB
Despite their potential as eco-friendly biofertilizers, the agricultural application of PSB faces several significant limitations. A major challenge is the inconsistency between laboratory success and field performance, which is heavily influenced by energy trade-offs and the "P-sink" effect (Raymond et al., 2021). Instead of solubilizing excess phosphorus for plants, PSB primarily mobilize P to fulfill their own metabolic requirements. In severely P-deficient soils, PSB can act as a sink, immobilizing P into their own microbial biomass and temporarily competing with plant roots for nutrients (Bargaz et al., 2021). Furthermore, secreting organic acids for P solubilization imposes a high energy cost on the bacteria. In natural soils, these acids have a short half-life and are quickly consumed by other microbes before effectively benefiting the plant.
Additionally, PSB activity is restricted by a negative feedback mechanism; existing soluble phosphate represses the genetic pathways (such as the gcd gene) responsible for organic acid synthesis (Zeng et al., 2016). This sensitivity makes it difficult to apply PSB alongside standard mineral fertilizers, as the presence of soluble P inhibits the bacteria's natural solubilization activity. Finally, environmental constraints dictate PSB efficacy. Their survival and solubilizing capacity are highly sensitive to abiotic stressors, including fluctuations in soil pH, temperature, moisture, and salinity (Sharma et al., 2013). Even under favorable conditions, introduced exogenous PSB must achieve rhizosphere competence while facing intense competition from the indigenous soil microbiome, which can lead to poor survival or disrupt native microbial ecosystems (Li et al., 2023).
While co-inoculating PSB with other microbial strains, such as AMF or nitrogen-fixing bacteria, is a common strategy intended to promote plant growth, the outcomes are not always positive or synergistic (Zhang et al., 2016; Nacoon et al., 2020). Research indicates several limitations and negative interactions when multiple strains are combined in the rhizosphere. Experiments combining PSB and AMF without the addition of external sparingly soluble phosphorus sources have demonstrated "less-than-additive" effects, indicating a complete lack of positive synergy between the microorganisms (Nacoon et al., 2020). The introduction of multiple microbes can lead to severe competition for nutrients. Under conditions of low phosphorus availability, for instance, PSB and AMF may directly compete with one another for the limited phosphorus pool rather than cooperating to feed the host plant (Zhang et al., 2016).
Furthermore, co-inoculation can result in antagonistic effects on microbial growth. Different PSB strains can exert strongly differential, and sometimes negative, effects on the growth of AMF extraradical hyphae (Ordoñez et al., 2016). Because of these potential trade-offs, researchers emphasize that multi-species consortia must be designed with extreme care to anticipate competitive exclusion, avoid microbial antagonism, and ensure true compatibility with both the host plant and the indigenous soil microbiome (De Zutter et al., 2022).
REGULATORY FRAMEWORK AND SPECIFICATION FOR PHOSPHATE SOLUBILIZING FERTILIZERS IN TAIWAN
According to Taiwan’s Fertilizer Management Act, fertilizers are explicitly defined as substances that supply nutrients to plants or enhance their utilization. In 2010, the Council of Agriculture (now the Ministry of Agriculture) revised the categories and specifications of fertilizers, formally incorporating microbial fertilizers into the national fertilizer regulatory framework (Li, 2012). The amendment added a category for microbial fertilizers, including six specific items: rhizobia microbial fertilizers, free-living nitrogen-fixing microbial fertilizers, phosphate-solubilizing microbial fertilizers, potassium-solubilizing microbial fertilizers, compound microbial fertilizers, and arbuscular mycorrhizal fungal fertilizers. This regulatory inclusion enabled fertilizer manufacturers to produce legally recognized microbial fertilizer products, marking the development of microbial fertilizers as a regulated and emerging industry.
Under the fertilizer categories and specifications, microbial fertilizers are defined as preparations containing active microorganisms or dormant spores—such as bacteria, actinomycetes, fungi, and algae —and their metabolic products, which are applied in crop production to supply nutrients or enhance nutrient uptake. Furthermore, all microorganisms used in microbial fertilizers must be naturally occurring in the environment or artificially induced through mutation, and must not include genetically modified microorganisms. When applying for registration certificates for manufacturing or importing microbial fertilizers, applicants must submit test reports on crop phytotoxicity, biological toxicity, and environmental ecological impact. In addition, microbial strains must comply with the safety assessment principles: “the strain exists naturally within the domestic environment,” “the strain is not associated with human diseases,” and “the strain is non-pathogenic to plants.”
Phosphate-solubilizing microbial fertilizers (Category No. 8-03) apply to products formulated with one or multiple strains capable of solubilizing phosphorus-containing inorganic minerals. These fertilizers may be in solid or liquid form. The main active ingredient must contain an effective viable count of at least 1×107 colony-forming units (CFU) per gram for solid formulations, or at least 1×108 CFU per milliliter for liquid formulations. Total nitrogen, total phosphorus pentoxide, or total potassium oxide contents exceeding 0.1% may be registered separately. Regarding harmful substances, arsenic must not exceed 25.0 mg kg-1, cadmium 2.0 mg kg-1, chromium 150 mg kg-1, copper 100 mg kg-1, mercury 1.0 mg kg-1, nickel 25.0 mg kg-1, lead 150 mg kg-1, and zinc 250 mg kg-1. Coliform bacteria must not exceed 1×103 MPN per gram (solid) or per milliliter (liquid). The contamination rate by non-target microorganisms must not exceed 15% for solid formulations or 5% for liquid formulations, and the moisture content of solid formulations must remain below 35.0%. Additionally, the product label must indicate phosphate-solubilizing activity (such as activity on tricalcium phosphate, aluminum phosphate, iron phosphate, or rock phosphate). A crop phytotoxicity test is also required, and only products demonstrating no phytotoxic effects may be registered. Microbial fertilizers that meet the material standards for organic certification may be selected and used by organic agricultural producers.
COMMERCIALIZATION OF PHOSPHATE SOLUBILIZING MICROBIAL FERTILIZERS IN TAIWAN
According to data retrieved from the “Integrated Fertilizer Management Information System” established by the Agriculture and Food Agency, Ministry of Agriculture, Taiwan, a total of 95 microbial fertilizer products have been registered to date. Among these, 89 products are phosphate-solubilizing microbial fertilizers, 3 are potassium-solubilizing microbial fertilizers, and 3 are arbuscular mycorrhizal fungal fertilizers, indicating that phosphate-solubilizing microbial fertilizers constitute the predominant category. There are 23 companies currently manufacturing phosphate-solubilizing microbial fertilizers. Across the 89 phosphate-solubilizing microbial fertilizer products, the registered microbial strains include Bacillus amyloliquefaciens, Bacillus licheniformis, Bacillus mycoides, Bacillus nitratireducens, Bacillus safensis, Bacillus siamensis, Bacillus subtilis, Bacillus velezensis, and Candida guilliermondii. Among these, Bacillus subtilis is the most widely commercialized, accounting for 29 products. This is followed by Bacillus amyloliquefaciens and Bacillus safensis, each represented by 19 products. Collectively, these three species constitute 76% of all phosphate-solubilizing microbial fertilizers.
Regarding product composition, 54% of phosphate-solubilizing microbial fertilizers consist solely of microbial powders or liquid cultures without the addition of chemical or organic fertilizers; 39% include chemical fertilizers, and 7% incorporate organic materials. By formulation type, 67% of products are in solid form, while 33% are liquid. At present, 73% of these products are listed in the recommended catalog of domestically produced microbial fertilizer brands, and 8% are included in the list of inputs approved for organic agriculture. Farmers may receive subsidies when purchasing phosphate-solubilizing microbial fertilizers included in these designated lists.
CONCLUSION
PSB can produce organic acids that solubilize sparingly soluble P compounds retained in soils, thereby increasing soil P availability and enhancing P accumulation in plant tissues. During strain selection, it is essential to test candidate isolates using various mineral P sources and identify those with superior organic acid-producing capacities. Subsequent inoculation trials can then be employed to obtain elite strains that effectively improve plant P uptake. In addition, the development and quality control of inoculant formulations play critical roles in ensuring product stability and consistent performance in soil environments.
Beyond increasing plant P content, PSB also promote plant growth through multiple mechanisms and can be incorporated into integrated plant nutrient management systems alongside mineral phosphate fertilizers and organic amendments. Such synergistic applications can enhance crop productivity while reducing the reliance on chemical fertilizers. Moreover, PSB may be combined with other PSB strains, arbuscular mycorrhizal fungi, or N-fixing bacteria to form beneficial microbial consortia.
The Taiwanese government has established a well-structured regulatory system for microbial fertilizers and ensures the production of high-quality products through rigorous review and inspection procedures. At present, PSB constitute the majority of registered microbial fertilizers in Taiwan, with Bacillus-based PSB products being particularly prevalent. In the future, efforts should focus on enhancing the effectiveness of microbial fertilizers in field applications. Supported by government-funded initiatives, efforts to advance the microbial fertilizer industry and promote field applications of microbial fertilizers are expected to continue.
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An Overview of Research on Phosphate-Solubilizing Bacteria and Their Commercialization Status in Taiwan
DOI: https://doi.org/10.56669/YTAX1606
ABSTRACT
Phosphorus (P) is an essential plant macronutrient; however, less than 1% of the total P content in global soils is available to plants due to widespread P fixation, wherein 75% to 90% of applied soluble inorganic fertilizers rapidly form insoluble complexes, often referred to as legacy P. This necessitates sustainable alternatives, given the energy-intensive nature of chemical fertilizer synthesis, the non-renewable status of phosphate rock, and the environmental risk of water eutrophication. Phosphate-solubilizing bacteria (PSB) offer an eco-friendly and biologically efficient strategy to enhance P utilization. P mobilization by PSB fundamentally relies on two pathways: mineral P solubilization and organic P mineralization. Solubilization of mineral P (e.g., tricalcium phosphate) is achieved primarily through the secretion of low-molecular-weight organic acids (such as gluconic acid). These acids chelate cations or release H+ ions, lowering the surrounding pH and converting fixed P into forms accessible to plants. Organic P is mineralized through the action of PSB-secreted enzymes, particularly phosphatases (acid, alkaline, and neutral) and phytases, which hydrolyze organic compounds to release orthophosphate. The genetic potential for these mechanisms is widespread, encompassing genes such as pqqE for acid secretion and phoD for alkaline phosphatase production. Beyond P mobilization, PSB strains are often multifunctional, promoting plant growth by producing phytohormones such as indole-3-acetic acid and 1-aminocyclopropane-1-carboxylate deaminase, and by producing siderophores. PSB are a vital component of integrated plant nutrient management systems. They exhibit synergistic effects when co-applied with sparingly soluble phosphate rock, organic amendments, or in multi-specific consortia alongside other PSB strains, arbuscular mycorrhizal fungi, or N-fixing bacteria. In Taiwan, PSB products constitute the predominant category of registered microbial fertilizers. The commercialized strains are mainly from the Bacillus genus, with B. subtilis, B. amyloliquefaciens, and B. safensis collectively representing 76% of registered products. Continued government support aims to advance the microbial fertilizer industry and reduce reliance on chemical inputs.
Keywords: phosphate-solubilizing bacteria, legacy P, organic acids, plant growth promotion, commercialization
INTRODUCTION
Phosphorus (P) is an essential plant macronutrient, ranking second in importance after nitrogen (N), and plays a crucial role in regulating agricultural production (Akplo et al., 2025). P is indispensable for plant development, involved in core metabolic processes such as cell division, energy production (ATP), macromolecule synthesis, signal transduction, and photosynthesis (Zhong et al., 2023).
Despite the relatively high total P content in global soils, generally ranging from 50–3000 mg kg-1, only a negligible amount (<1%) is available to plants (Richardson et al., 2009; Akplo et al., 2025). The primary challenge arises from the widespread phenomenon of P fixation or immobilization, in which 75% to 90% of applied soluble inorganic fertilizers rapidly bind to metal cations (Ca, Al, Fe), forming insoluble complexes that plants cannot utilize (Sharma et al., 2013). This accumulated, fixed P is often referred to as legacy P (Némery and Garnier, 2016; Li et al., 2023).
The necessity for sustainable alternatives is driven by multiple factors, including the highly energy-intensive processes involved in chemical fertilizer synthesis, the non-renewable nature of phosphate rock resources, and the environmental risks associated with excessive P runoff, particularly water eutrophication (Mueller et al., 2012; Sharma et al., 2013). Phosphate-solubilizing microorganisms (PSM) offer an eco-friendly, low-cost, and biologically efficient strategy to enhance P utilization efficiency in sustainable cropping systems (Timofeeva et al., 2022).
PHYLOGENETIC AND ECOLOGICAL DISTRIBUTION OF PSB
Among the whole microbial population in soil, phosphate-solubilizing bacteria (PSB) comprise 1–50% and phosphate-solubilizing fungi (PSF) 0.1 to 0.5% of the total respective population (Kalayu, 2019). According to recent studies, the currently known PSB strains are generally members of three phyla: Actinomycetota (Actinobacteria), Bacillota (Firmicutes), and Pseudomonadota (Proteobacteria). At the genus level, PSB strains have been classified within the genera Acinetobacter, Aeromonas, Agrobacterium, Alcaligenes, Arthrobacter, Azotobacter, Bacillus, Bradyrhizobium, Burkholderia, Citrobacter, Cyanobacteria, Delftia, Enterobacter, Erwinia, Gordonia, Klebsiella, Kushneria, Micrococcus, Paenibacillus, Pantoea, Phyllobacterium, Pseudomonas, Rhizobium, Rhodococcus, Salmonella, Serratia, Sinomonas, Sphingobium, Streptomyces, Thiobacillus, and Xanthomonas (Timofeeva et al., 2022; Li et al., 2023).
The ecological niches of PSB encompass diverse habitats, including general soil environments; the rhizospheres of corn, rice, wheat, cowpea, grass, oil palm, spiny deciduous shrub, and giant cardon cactus; lateritic soils; acid sulfate soils; calcareous soils; tropical and subtropical soils; mangrove ecosystems; wheat grains; as well as P-rich substrates such as Indian rock phosphate and Venezuelan phosphate rocks (Song et al., 2022; Timofeeva et al., 2022).
MECHANISMS OF PHOSPHATE MOBILIZATION
P mobilization is fundamentally achieved through mineral P solubilization and organic P mineralization, and the physiological and molecular mechanisms involved are summarized below.
Mineral P solubilization
Physiological mechanisms
Mineral P sources such as tricalcium phosphate (Ca3(PO4)2), aluminum phosphate (AlPO4), and iron phosphate (FePO4) can be utilized by solubilizing action of acids and chelation. It is widely recognized that PSB secrete low-molecular-weight organic acids, which chelate cations bound to phosphate via their hydroxyl and carboxyl groups, or release H+ ions that lower the surrounding pH (Chen et al., 2006; Lin et al., 2006; Li et al., 2023). These processes convert fixed P into a form that plants can readily access. The predominant organic acids produced by PSB and involved in P-solubilization include acetic acid, ascorbic acid, butyric acid, citric acid, formic acid, gluconic acid, isobutyric acid, isovaleric acid, 2-ketogluconic acid, lactic acid, malic acid, oxalic acid, oxyglutaric acid, propanedioic acid, propionic acid, pyruvic acid, succinic acid, and tartaric acid (Li et al., 2023).
Molecular mechanisms
Many genes involved in acid secretion that enhance the solubilization of mineral P through genetic manipulation have been studied (Li et al., 2023). Researchers cloned the Erwinia herbicola pyrroloquinoline quinone (PQQ) synthase gene into Escherichia coli HB101, enabling the bacteria to synthesize PQQ (Liu et al., 1992). This cofactor activates glucose dehydrogenase, enabling Escherichia coli to convert glucose into gluconic acid, thereby increasing acid secretion and improving the solubility of mineral P. Amino acid sequence alignment data from several bacterial species showed that the pqqE gene is highly conserved and is a hallmark gene in hydroxyapatite solubilization (Ludueña et al., 2016). Introducing the 396-base gabY gene from Pseudomonas cepacia into Escherichia coli JM109 was enough to trigger the mineral P solubilization and gluconic acid production (Babu-Khan et al., 1995). Although gabY does not resemble known direct-oxidation pathway genes, its predicted protein shares substantial sequence similarity with membrane proteins of the histidine permease (HisQ) family. In addition, a DNA fragment from Serratia marcescens was shown to induce gluconic acid synthesis in Escherichia coli DH5α, but it does not exhibit any homology to the previously characterized genes (Krishnaraj and Goldstein, 2001).
Organic P mineralization
Physiological mechanisms
Organic matter represents the second major pool of soil P, with organic P generally comprising 30–50% of total soil P. Most organic P is found as inositol phosphate (phytate), while additional forms include phosphomonoesters, phosphodiesters including phospholipids and nucleic acids, and phosphotriesters (Rodríguez and Fraga, 1999). The mineralization of organic P by enzymes secreted by PSB represents a major dephosphorylation pathway, primarily mediated by phosphatase, phytases, and C-P-cleaving enzymes (Pan and Cai, 2023). Phosphatases are classified as acidic, alkaline, or neutral. Acid phosphatases are most effective in mineralizing organic P in acidic soils, whereas alkaline phosphatases primarily hydrolyze phospholipids and release orthophosphate in alkaline soils. Neutral phosphatases exhibit comparatively limited activity in P mineralization. Phytase mineralizes phytate-bound organic P, producing intermediates that phosphatases can further hydrolyze to release orthophosphate, since phytate’s ester bonds are otherwise too stable to break (Pan and Cai, 2023).
Molecular mechanisms
Many of the genes in PSB encode different enzymes, such as alkaline phosphatases (phoA, phoD, phoX), acid phosphatases (phoC), phytase (appA), C-P cleavage enzyme (phn), extracellular polyphosphatase (ppx), and polyphosphate kinase (ppk), with alkaline phosphatases being the most studied (Pan and Cai, 2023). Under inorganic P limitation, bacteria activate the P starvation (Pho) regulon and induce alkaline phosphatase production, enabling energy-efficient enzyme synthesis and switching P uptake to an alternative transport system (Vershinina and Znamenskaya, 2002). Three homologous genes—phoA, phoD, and phoX—associated with alkaline phosphatase production have been identified within the Pho regulon, and 31.9% of 3,058 sequenced prokaryotic genomes possess at least one of these genes, indicating broad genetic potential for alkaline phosphatase synthesis (Zimmerman et al., 2013). In soil bacteria, phoD was the most frequently detected alkaline phosphatase gene in 16S rRNA-associated metagenomic datasets, with phoA and phoX also detected (Tan et al., 2013). Although phoA was initially thought to be the primary source of alkaline phosphatase in marine ecosystems, more recent findings indicate that phoX is more widely distributed among marine bacteria and is induced exclusively under P starvation (Sebastian and Ammerman, 2009). PafA is a phosphate-insensitive phosphatase widely distributed in Bacteroidota (Bacteroidetes) and abundant in natural environments, where it plays a major role in regenerating phosphate (Lidbury et al., 2022). The pafA gene is highly diverse in plant rhizospheres, and it is abundant in the global ocean, where it is expressed independently of P availability.
ADVANCES AND CHALLENGES IN SCREENING AND FORMULATION OF PSB
The key developments in screening potential PSB are outlined, and the remaining challenges in inoculant formulation and quality control are highlighted.
Optimization of liquid medium formulation
Historically, PSB isolation relied on the halo/zone assay on Pikovskaya solid medium (PVK) (Pikovskaya, 1948). Later, a newly formulated medium, the National Botanical Research Institute’s phosphate growth medium (NBRIP), was adopted, which enabled the detection of about 3-fold higher phosphate-solubilizing activity in broth assay compared to PVK (Nautiyal, 1999). Using this improved formulation for phosphate solubilization assays, it demonstrated that many bacterial strains that did not form a visible halo/zone on agar plates could still exhibit measurable phosphate-solubilizing activity in liquid medium. Therefore, the NBRIP broth assay provides a more effective approach for screening for the most efficient PSB.
Rapid visual test for PSB
An efficient visual method was established for the qualitative screening of PSB (Mehta and Nautiyal, 2001). The incorporation of bromophenol blue allows for rapid qualitative detection of strains capable of solubilizing P. The formulation can also be used as a quality control test to expeditiously screen commercial bioinoculant preparations based on P solubilizers.
Guidelines used for isolating and testing PSB
Reviews of the literature and chemical considerations related to phosphate solubilization by microorganisms have shown that the commonly used selection factor for this trait, tricalcium phosphate (Chen et al., 2006), is relatively weak and unreliable as a universal selection factor for isolating and testing PSB for enhancing plant growth (Bashan et al., 2013a). Consequently, Bashan et al. (2013b) proposed a set of guidelines for identifying PSB with real agronomic potential, providing a more reliable framework for their evaluation. These guidelines are summarized below.
A combination of two or three metal-P compounds, when used together or in tandem, should replace the sole tricalcium as an initial selection factor. The selection of metal-P candidates for potential PSB will depend on the soil type where the PSB will be used. Adding other Ca-P compounds, such as rock phosphates for alkaline soils, Al-P and Fe-P compounds for acidic soils, is suggested.
The few bacterial isolates that are positive in both the halo/zone assay and broth assay should be further tested for abundant production of organic acids.
Isolates complying with the above criteria should be tested on a model plant as the ultimate test for potential P solubilization. Parameters related to P nutrition in plants should be tested, not growth promotion in general, because growth promotion can result from other mechanisms.
Inoculant formulation
The transfer from laboratory efficacy to commercial success requires a robust inoculant formulation. Inoculant carriers can be divided into five basic categories: (1) Soils: peat, coal, clays, and inorganic soil, (2) Waste plant materials of diverse agriculture origins: lignin, soybean or wheat bran, grape bagasse and banana waste, (3) Inert materials: polymers, treated rock fragments such as vermiculite and perlite, (4) Plain lyophilized microbial cultures and oil-dried bacteria that can later be incorporated into a solid carrier or used as they are, and (5) Liquid inoculants, where chemicals such as carboxymethyl cellulose, glycerol, trehalose, gum Arabic, were added to the liquid medium to improve stickiness, stabilization, surfactant, function, and dispersal (Bashan et al., 2014). Although no ideal formulation exists and each type presents distinct strengths and limitations, certain key steps in inoculant production require careful attention (Herrmann and Lesueur, 2013). Choices made during these steps ultimately dictate the success or failure of inoculation. Regardless of the specific formulation, the final inoculant can be of four types: liquid, slurry, granular, or powder. Any formulation must be stable during production, distribution, storage, and transportation to the farmer, particularly when the main ingredient is alive and susceptible to changes.
Quality control
Many inoculants currently available in the market are of poor quality, leading to a loss of confidence among farmers. Practical methods for the quality control of inoculant biofertilizers have been proposed by the Australian Centre for International Agricultural Research (ACIAR) (Deaker et al., 2011). Quality control should verify that there are sufficient viable numbers of the correct strains of microorganisms in the biofertilizer throughout the product's shelf life. Farm trials should also be part of quality control, demonstrating that the biofertilizer actually increases crop yield while reducing chemical fertilizer inputs. A high-quality inoculant must satisfy both farmers and producers by containing a large number of one or more strains that deliver maximal, consistent, and reproducible performance across varying field environments; remaining free from major contaminants and opportunistic pathogens affecting humans, animals, or plants; and maintaining an extended shelf life capable of tolerating typical on-farm handling (Herrmann and Lesueur, 2013).
MULTIFUNCTIONALITY AND GROWTH-PROMOTING POTENTIAL OF PSB
Plant growth-promoting traits
Beyond P solubilization, PSB often possess the ability to modify root functioning to enhance P acquisition through bacterial plant growth-promoting activities (Bargaz et al., 2021; Chen et al., 2021).
Phytohormone production: PSB inoculation can increase the germination percentage of seeds by secreting indole-3-acetic acid (IAA), hence playing a major role in the regulation of endogenous IAA level with positive consequences on P acquisition and plant physiological status (Song et al., 2022).
1-aminocyclopropane-1-carboxylate (ACC) deaminase activity: The root length and root biomass of rice plants strongly correlated with ACC deaminase produced by Alcaligenes sp. with P-solubilizing trait, and led to improved shoot growth (Bal et al., 2013).
Nitrogen fixation: The main advantage of PSB with N-fixing activity is their beneficial nutritional effect resulting from both P mobilization and N fixation (Peix et al., 2001).
Siderophore production: PSB can mobilize Fe–P via siderophore production, thereby facilitating the conversion of insoluble P and Fe into more available forms (Cui et al., 2022).
PSB as a biofertilizer for diverse crop species
As a member of plant growth-promoting rhizobacteria, PSB can promote plant growth through a wide range of mechanisms, and its agricultural potential continues to increase as it provides an appealing alternative to chemical fertilizers. For example, inoculation with the two auxin-producing PSB increased both P concentration and auxin levels in wheat plants, resulting in greater plant biomass (Kudoyarova et al., 2017). This highlights the importance of elevated auxin content in stimulating root growth and enhancing P uptake capacity in response to PSB. The P-solubilizing and IAA-producing Paenibacillus sp. B1 significantly increased maize root and shoot length, enhanced phosphorus and nitrogen uptake, and raised total dry biomass (Li et al., 2017). The growth-promoting effects of PSB have been demonstrated across a broad range of crop categories, including cereals (wheat, maize, sorghum, rice, barley), legumes (peanut, soybean, beans, chickpea), oilseed crops (canola), root and tuber crops (potato, radish, sugar beet), vegetables (lettuce, tomato), fruit crops (apple, citrus), industrial crops (sugarcane), and various ornamental plants (Kalayu, 2019).
AGRONOMIC INTEGRATION AND COMPLEX MICROBIAL INTERACTIONS
Integrated nutrient management and legacy P utilization
PSB serve as a vital component in an integrated plant nutrient management system (IPNMS), maximizing the efficiency of applied and native P sources (Bargaz et al., 2018). The combined use of microbial and mineral resources is an emerging research area that aims to develop efficient microbial formulations compatible with mineral inputs, with positive effects on both crops and the environment.
Synergy with P fertilizers: Microbial-based bioformulations that increase plant performance and exhibit complementary and synergistic effects with mineral fertilization are greatly needed (Bargaz et al., 2018). Co-applications of elite PSB strains with sparingly soluble rock phosphate or tricalcium phosphate have been demonstrated to increase available P content in the soil as well as plant P uptake and plant biomass in the pot experiment and field trial (Kaur and Reddy, 2015; Zineb et al., 2020; Song et al., 2022).
Organic amendments: PSB synergize effectively with organic amendments such as cow dung manure, which improved P content and growth of Brassica juncea (Singh et al., 2014). The combined application of bio-organic phosphate and the PSB significantly enhanced the growth, yield parameters, and productivity of two wheat cultivars compared to non-inoculated control treatments (Tahir et al., 2018). A study demonstrated that partial replacement of mineral P with organic manure could reshape the phosphate-solubilizing and alkaline phosphomonoesterase-producing bacterial communities, making them more resilient and effective for high P utilization and productivity under intensive cultivation (Bi et al., 2020).
Legacy P activation: Global agricultural soils contain enough accumulated P to support crop production for roughly a century. Consequently, researchers have explored the potential of soil “P activators” to mobilize this legacy P for plant use (Zhu et al., 2018; Li et al., 2023). Although results have varied, growing evidence indicates that these activators can increase soil phosphate availability and help alleviate the global P crisis.
Microbial consortia and multi-species interactions
Single-strain inoculation often yields inconsistent field results due to competition and environmental variability. Using multi-specific consortia is generally considered a more robust approach (Zineb et al., 2020).
PSB consortia: The pot experiment illustrated that available P in the soil, as well as plant P uptake, could be improved with inoculation of a mixture of PSB (Song et al., 2022). Inoculating plants with P-efficient bacterial consortia is an emerging research area that requires attention to identify microbial combinations that can enhance both above- and below-ground performance, thereby increasing plant growth and yield (Bargaz et al., 2021).
PSB and Arbuscular mycorrhizal fungi (AMF): In a study on the interactions between PSB and AMF, it was found that AMF affected the growth of different PSB strains, and the other bacterial strains also had substantial effects on the development of AMF extraradical hyphae outside carrot roots and on the colonization of potato roots by AMF (Ordoñez et al., 2016). Dual inoculation with PSB and AMF enhanced plant biomass and nutrient (N and P) accumulation, likely because PSB released phosphate that AMF efficiently absorbed (Toro et al., 1997). These interactions between bacteria and fungi supported P cycling and provided a more sustainable nutrient supply for plants. A synergetic effect of PSB, AMF, and phosphor-compost was demonstrated in tomato seedlings, which showed enhancement in P solubilization and plant growth (El Maaloum et al., 2020).
PSB and diazotrophs: Co-inoculation of PSB and mixed rhizobial culture significantly enhanced the plant growth, shoot P and N concentrations, nodulation efficiency, and nitrogenase activity (Gull et al., 2004). Dual inoculation with PSB (Pseudomonas) and N-fixing bacteria (Bradyrhizobium) significantly enhanced symbiotic nitrogen fixation, nutrient acquisition, and soybean growth in pot and field experiments (Tu et al., 2021; Kumawat et al., 2022).
LIMITATIONS IN THE AGRICULTURAL APPLICATION OF PSB
Despite their potential as eco-friendly biofertilizers, the agricultural application of PSB faces several significant limitations. A major challenge is the inconsistency between laboratory success and field performance, which is heavily influenced by energy trade-offs and the "P-sink" effect (Raymond et al., 2021). Instead of solubilizing excess phosphorus for plants, PSB primarily mobilize P to fulfill their own metabolic requirements. In severely P-deficient soils, PSB can act as a sink, immobilizing P into their own microbial biomass and temporarily competing with plant roots for nutrients (Bargaz et al., 2021). Furthermore, secreting organic acids for P solubilization imposes a high energy cost on the bacteria. In natural soils, these acids have a short half-life and are quickly consumed by other microbes before effectively benefiting the plant.
Additionally, PSB activity is restricted by a negative feedback mechanism; existing soluble phosphate represses the genetic pathways (such as the gcd gene) responsible for organic acid synthesis (Zeng et al., 2016). This sensitivity makes it difficult to apply PSB alongside standard mineral fertilizers, as the presence of soluble P inhibits the bacteria's natural solubilization activity. Finally, environmental constraints dictate PSB efficacy. Their survival and solubilizing capacity are highly sensitive to abiotic stressors, including fluctuations in soil pH, temperature, moisture, and salinity (Sharma et al., 2013). Even under favorable conditions, introduced exogenous PSB must achieve rhizosphere competence while facing intense competition from the indigenous soil microbiome, which can lead to poor survival or disrupt native microbial ecosystems (Li et al., 2023).
While co-inoculating PSB with other microbial strains, such as AMF or nitrogen-fixing bacteria, is a common strategy intended to promote plant growth, the outcomes are not always positive or synergistic (Zhang et al., 2016; Nacoon et al., 2020). Research indicates several limitations and negative interactions when multiple strains are combined in the rhizosphere. Experiments combining PSB and AMF without the addition of external sparingly soluble phosphorus sources have demonstrated "less-than-additive" effects, indicating a complete lack of positive synergy between the microorganisms (Nacoon et al., 2020). The introduction of multiple microbes can lead to severe competition for nutrients. Under conditions of low phosphorus availability, for instance, PSB and AMF may directly compete with one another for the limited phosphorus pool rather than cooperating to feed the host plant (Zhang et al., 2016).
Furthermore, co-inoculation can result in antagonistic effects on microbial growth. Different PSB strains can exert strongly differential, and sometimes negative, effects on the growth of AMF extraradical hyphae (Ordoñez et al., 2016). Because of these potential trade-offs, researchers emphasize that multi-species consortia must be designed with extreme care to anticipate competitive exclusion, avoid microbial antagonism, and ensure true compatibility with both the host plant and the indigenous soil microbiome (De Zutter et al., 2022).
REGULATORY FRAMEWORK AND SPECIFICATION FOR PHOSPHATE SOLUBILIZING FERTILIZERS IN TAIWAN
According to Taiwan’s Fertilizer Management Act, fertilizers are explicitly defined as substances that supply nutrients to plants or enhance their utilization. In 2010, the Council of Agriculture (now the Ministry of Agriculture) revised the categories and specifications of fertilizers, formally incorporating microbial fertilizers into the national fertilizer regulatory framework (Li, 2012). The amendment added a category for microbial fertilizers, including six specific items: rhizobia microbial fertilizers, free-living nitrogen-fixing microbial fertilizers, phosphate-solubilizing microbial fertilizers, potassium-solubilizing microbial fertilizers, compound microbial fertilizers, and arbuscular mycorrhizal fungal fertilizers. This regulatory inclusion enabled fertilizer manufacturers to produce legally recognized microbial fertilizer products, marking the development of microbial fertilizers as a regulated and emerging industry.
Under the fertilizer categories and specifications, microbial fertilizers are defined as preparations containing active microorganisms or dormant spores—such as bacteria, actinomycetes, fungi, and algae —and their metabolic products, which are applied in crop production to supply nutrients or enhance nutrient uptake. Furthermore, all microorganisms used in microbial fertilizers must be naturally occurring in the environment or artificially induced through mutation, and must not include genetically modified microorganisms. When applying for registration certificates for manufacturing or importing microbial fertilizers, applicants must submit test reports on crop phytotoxicity, biological toxicity, and environmental ecological impact. In addition, microbial strains must comply with the safety assessment principles: “the strain exists naturally within the domestic environment,” “the strain is not associated with human diseases,” and “the strain is non-pathogenic to plants.”
Phosphate-solubilizing microbial fertilizers (Category No. 8-03) apply to products formulated with one or multiple strains capable of solubilizing phosphorus-containing inorganic minerals. These fertilizers may be in solid or liquid form. The main active ingredient must contain an effective viable count of at least 1×107 colony-forming units (CFU) per gram for solid formulations, or at least 1×108 CFU per milliliter for liquid formulations. Total nitrogen, total phosphorus pentoxide, or total potassium oxide contents exceeding 0.1% may be registered separately. Regarding harmful substances, arsenic must not exceed 25.0 mg kg-1, cadmium 2.0 mg kg-1, chromium 150 mg kg-1, copper 100 mg kg-1, mercury 1.0 mg kg-1, nickel 25.0 mg kg-1, lead 150 mg kg-1, and zinc 250 mg kg-1. Coliform bacteria must not exceed 1×103 MPN per gram (solid) or per milliliter (liquid). The contamination rate by non-target microorganisms must not exceed 15% for solid formulations or 5% for liquid formulations, and the moisture content of solid formulations must remain below 35.0%. Additionally, the product label must indicate phosphate-solubilizing activity (such as activity on tricalcium phosphate, aluminum phosphate, iron phosphate, or rock phosphate). A crop phytotoxicity test is also required, and only products demonstrating no phytotoxic effects may be registered. Microbial fertilizers that meet the material standards for organic certification may be selected and used by organic agricultural producers.
COMMERCIALIZATION OF PHOSPHATE SOLUBILIZING MICROBIAL FERTILIZERS IN TAIWAN
According to data retrieved from the “Integrated Fertilizer Management Information System” established by the Agriculture and Food Agency, Ministry of Agriculture, Taiwan, a total of 95 microbial fertilizer products have been registered to date. Among these, 89 products are phosphate-solubilizing microbial fertilizers, 3 are potassium-solubilizing microbial fertilizers, and 3 are arbuscular mycorrhizal fungal fertilizers, indicating that phosphate-solubilizing microbial fertilizers constitute the predominant category. There are 23 companies currently manufacturing phosphate-solubilizing microbial fertilizers. Across the 89 phosphate-solubilizing microbial fertilizer products, the registered microbial strains include Bacillus amyloliquefaciens, Bacillus licheniformis, Bacillus mycoides, Bacillus nitratireducens, Bacillus safensis, Bacillus siamensis, Bacillus subtilis, Bacillus velezensis, and Candida guilliermondii. Among these, Bacillus subtilis is the most widely commercialized, accounting for 29 products. This is followed by Bacillus amyloliquefaciens and Bacillus safensis, each represented by 19 products. Collectively, these three species constitute 76% of all phosphate-solubilizing microbial fertilizers.
Regarding product composition, 54% of phosphate-solubilizing microbial fertilizers consist solely of microbial powders or liquid cultures without the addition of chemical or organic fertilizers; 39% include chemical fertilizers, and 7% incorporate organic materials. By formulation type, 67% of products are in solid form, while 33% are liquid. At present, 73% of these products are listed in the recommended catalog of domestically produced microbial fertilizer brands, and 8% are included in the list of inputs approved for organic agriculture. Farmers may receive subsidies when purchasing phosphate-solubilizing microbial fertilizers included in these designated lists.
CONCLUSION
PSB can produce organic acids that solubilize sparingly soluble P compounds retained in soils, thereby increasing soil P availability and enhancing P accumulation in plant tissues. During strain selection, it is essential to test candidate isolates using various mineral P sources and identify those with superior organic acid-producing capacities. Subsequent inoculation trials can then be employed to obtain elite strains that effectively improve plant P uptake. In addition, the development and quality control of inoculant formulations play critical roles in ensuring product stability and consistent performance in soil environments.
Beyond increasing plant P content, PSB also promote plant growth through multiple mechanisms and can be incorporated into integrated plant nutrient management systems alongside mineral phosphate fertilizers and organic amendments. Such synergistic applications can enhance crop productivity while reducing the reliance on chemical fertilizers. Moreover, PSB may be combined with other PSB strains, arbuscular mycorrhizal fungi, or N-fixing bacteria to form beneficial microbial consortia.
The Taiwanese government has established a well-structured regulatory system for microbial fertilizers and ensures the production of high-quality products through rigorous review and inspection procedures. At present, PSB constitute the majority of registered microbial fertilizers in Taiwan, with Bacillus-based PSB products being particularly prevalent. In the future, efforts should focus on enhancing the effectiveness of microbial fertilizers in field applications. Supported by government-funded initiatives, efforts to advance the microbial fertilizer industry and promote field applications of microbial fertilizers are expected to continue.
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