Skip to main content
NCBI home page
Current Research in Microbial Sciences logoLink to Current Research in Microbial Sciences
. 2024 Nov 27;8:100326. doi: 10.1016/j.crmicr.2024.100326

Phosphorus dynamics and sustainable agriculture: The role of microbial solubilization and innovations in nutrient management

José Abraham García-Berumen a, Juan Armando Flores de la Torre b, Sergio de los Santos-Villalobos c, Alejandro Espinoza-Canales a, Francisco Guadalupe Echavarría-Cháirez d, Héctor Gutiérrez-Bañuelos a,⁎
PMCID: PMC11647644  PMID: 39687549

Highlights

  • •

    Phosphorus-solubilizing microorganisms (PSMs) are beneficial microorganisms that can convert insoluble phosphorus (P) into forms available for plant uptake, enhancing soil fertility and crop productivity.

  • •

    PSMs secrete organic acids (e.g., citric, gluconic, and oxalic acids) that chelate cations bound to phosphate, releasing soluble P.

  • •

    Enzymes such as phosphatases and phytases are produced by PSMs, aiding in the mineralization of organic phosphorus compounds.

  • •

    Utilizing PSMs can decrease the need for chemical P fertilizers, as the development of microbial inoculants lowers agricultural costs and environmental impact.

  • •

    PSMs maintain soil health by improving nutrient cycling and increasing soil microbial diversity.

  • •

    By enhancing P-use efficiency, PSMs can reduce phosphorus runoff into water bodies, thereby minimizing eutrophication and water pollution.

Keywords: Phosphorus, Phosphate rock, Phosphorus-solubilizing microorganisms, Sustainable agriculture

Abstract

Phosphorus (P) is an essential element for plant growth, playing a crucial role in various metabolic processes. Despite its importance, phosphorus availability in soils is often restricted due to its tendency to form insoluble complexes, limiting plant uptake. The increasing demand for phosphorus in agriculture, combined with limited global reserves of phosphate rock, has created challenges for sustainable plant production. Additionally, the overuse of chemical phosphorus fertilizers has resulted in environmental degradation, such as eutrophication of water bodies. Increasing agronomic phosphorus (P) efficiency is crucial because of population growth and increased food demand. Hence, microorganisms involved in the P cycle are a promising biotechnological strategy that has gained global interest in recent decades. Microorganisms' solubilization of phosphate rock (PR) is an environmentally sustainable alternative to chemical processing for producing phosphate fertilizers. Phosphorus-solubilizing microorganisms (PSMs), including bacteria and fungi, and their enzymatic processes offer an eco-friendly and sustainable alternative to chemical inputs by converting insoluble phosphorus into forms readily available for plant uptake. Integrating PSMs into agricultural systems presents a promising strategy to reduce dependence on chemical fertilizers, enhance soil health, and contribute to the transition toward more sustainable and resilient agricultural practices. It can be an alternative that reduces the loss of phosphorus in the environment, especially the eutrophication of aquatic systems. This paper explores the challenges of phosphorus availability in agriculture and the potential of microbial phosphorus solubilization as a sustainable alternative to conventional practices.

Graphical abstract

Image, graphical abstract

Open in a new tab

Introduction

Phosphorus (P) is a crucial macronutrient that plants require in high amounts. It plays an essential role in forming DNA, generating ATP and NADPH (in catabolic processes), and influencing photosynthesis, respiration, and protein synthesis rates (Kumar and Mohapatra, 2021). One of the roles of P-solubilizing microorganisms is to break down non-solubilizing tricalcium phosphate or rock phosphate forms so that plants can uptake P (Rawat et al., 2021). In many crop production systems, available P has been the primary factor limiting plant growth rates (P is the most common limiting nutrient in crop production). Soil deficiencies of phosphorus are traditionally solved by using inorganic phosphate fertilizers; however, using large amounts of these fertilizers is uneconomical and poses significant environmental risks (Cordell and White, 2014). Economic efficacy concerns and the apprehension of high levels of P in the aquifers have led ecologists to investigate the links between P bioaccumulation in water ecosystems and P levels in the soil to find long-lasting and effective alternatives to the use of P fertilizers (McMahon and Read, 2013; Alewell et al., 2020).

The alternative of using PSMs to access insoluble forms of P compounds allows plants to uptake more phosphorus and minimizes the side effects on the environment (Silva et al., 2023). PSMs are ubiquitous and an essential component of the biogeochemical P cycle because phosphate mobilization occurs in many natural (eutrophic lakes and oceans) and extreme environments (volcanic, marine sediments, and deserts). These microorganisms are mainly bacteria and fungi, known for their ability to solubilize hardly soluble phosphates (Tian et al., 2021). Several PSMs tend to produce alkalinizing organic acids (such as citric, lactic, gluconic, tartaric, formic, acetic, and oxalic acid), which have high affinities for aluminum and calcium, the primary metal ions that form insoluble aluminum and calcium phosphates in the soils (Varga et al., 2020). They also have the extraordinary ability to form chelates of Fe released from insoluble Fe forms to enhance their phosphorus colonization. These arguing capacities are beneficial to the plants, which absorb nourishment through their roots, directed by complex signals released by the microorganisms, such as water, pH, nutrients, chemical signals, root exudates, and plant growth inhibitors (Wang et al., 2021). Another mechanism includes enzyme secretion and complex population dynamics (Rawat et al., 2021).

PSMs are an essential link between the geosphere, hydrosphere, and biosphere. They deliver P to plants by intercepting the dissolved P and mineralizing P carried into the soil by the weather (Liu, 2021). The soil type has a significant effect on the ability of the PSMs. Several researchers (Dissanayaka et al., 2021; Wang et al., 2021) have found that the growth of phosphorus-solubilizing bacteria and fungi tends to be higher in acidic soils (pH 5.0 to 6.5) than in alkaline soils, with bacterial growth also limited in alkaline soils (pH above 7.0). Consequently, the actual populations and variety of PSMs in the soil are influenced by the site´s numerous biotic and abiotic features, such as physical, chemical, and ecological factors (Dey et al., 2021). The PSMs exert various plant-promoting effects, making added organic phosphorus more available to plants (Rawat et al., 2021). Their use offers an environmentally friendly and biologically more sustainable alternative for long-term success and sustainable agriculture (Pang et al., 2024; Silva et al., 2023). The growing interest in this group of microbes is not exclusively due to their capability of solubilizing insoluble forms of phosphorus but also to the use of plant growth-promoting Rhizobacteria and plant growth-promoting Rhizophagous fungi to enhance the health of plants and crop yield (Varga et al., 2020). This review aims to provide an overview of challenges associated with phosphorus availability in agriculture systems, and to investigate the potential of microbial PSMs and their enzymatic processes in enhancing phosphorus bioavailability, while also examining sustainable strategies, such as the development of microbial inoculants, to improve phosphorus use efficiency and reduce environmental impacts in agriculture.

Phosphorus, an essential element for the plant nutrition and food production

Phosphorus (P) is one of the 17 essential elements for plant growth and is crucial for a range of metabolic processes. These include energy generation, nucleic acid synthesis, photosynthesis, glycolysis, respiration, membrane synthesis and stability, enzyme activation/inactivation, redox reactions, signaling, carbohydrate metabolism, and nitrogen fixation (Vance et al., 2003). Moreover, phosphorus is involved primarily in core and important molecules for living organisms, including DNA, RNA, sugar, lipids, proteins, ATP, ADP, and NADPH (Zhang et al., 2014).

Agronomically, after nitrogen, phosphorus is the second limiting nutrient for the development and growth of plants since the concentration of P reaches up to 0.5 % of the dry weight of the plant (Vance et al., 2003). Phosphorus rock minerals are the only phosphorus resources in the world, and these advantages come at a significant cost (Geissler et al., 2018). Mobilizing phosphate rock into the environment faster altered the global phosphorus cycle by mobilizing four times the natural level of phosphorus from phosphate rock into the environment (Alewell et al., 2020). This has not only contaminated many of the world's freshwater bodies and oceans but also created human dependence on a single non-renewable resource and contributed to widespread nutrient pollution of many of the world's lakes, rivers, and oceans. Additionally, the depletion of this finite resource, which took tens of millions of years to form, is a concern (Filippelli, 2008; World Resources Institute, 2008).

Chemist and science writer Isaac Asimov described phosphorus as “the bottleneck of life” and warned 30 years ago: “Perhaps we can replace coal with nuclear energy, wood with plastics, meat with yeast and isolation for friendship, but for phosphorus, there is no substitute or replacement” (Asimov, 1974).

Achieving global food security means ensuring that food is available, accessible, and nutritious for all people at all times (FAO, 2023). However, this is likely one of the most significant challenges of the 21st century. At the same time, food demand is expected to double to feed 9 billion mouths by 2050 (Roser and Richie, 2023). Many of the essential resources that support food production are increasingly scarce. Food can only be produced with access to water, energy, land, and nutrients. However, unlike water scarcity, energy limitation, and nitrogen management, soil loss through erosion and dwindling phosphorus availability represent one of the most significant regional and global challenges to sustaining food production (Alewell et al., 2020).

Phosphorus remains essential in food production. Thanks to phosphate fertilizers, crop yields have increased in the last 50 years and contributed to the world population (Cordell and White, 2011).

The significance of phosphorus in crop growth was established as far back as 1840 by Liebig, who identified phosphorus as the limiting nutrient in plant growth, which led to the collection and grinding of bones for their high phosphate value and the discovery of guano as another phosphate source (Salgado Garcia et al., 2012). Large deposits of phosphate-rich rocks were also found in the United States, which could be easily mined for their fertilizer value (PotashCorp, 2011). Historically, crop production relied on natural soil phosphorus levels, supplemented by organic sources such as manure, crop residues, and human excrement (Timsina, 2018). The post-World War II era, marked by population growth, hunger, and urbanization, spurred the Green Revolution to increase crop productivity through new crop varieties and synthetic fertilizers (John and Babu, 2021). Phosphate rock extraction increased rapidly to keep up with nitrogen production through the Haber-Bosch process (FAO, 2022).

Currently, commercial fertilizers are multiple and could be found as simple fertilizers when only a single nutrient is present, such as superphosphate or triple super phosphate, such as urea or ammonium sulfate for simple nitrogen fertilizers, while ammonium phosphate (MAP), ammonium diphosphate (DAP), nitro phosphate (NP) and NPK, among other fertilizers, those that contain more of an essential nutrient. Improving agricultural productivity to guarantee food security is a cause for concern since it will undoubtedly require adequate raw materials to produce these essential nutrients, including P (Castro and Melgar, 2005).

Fertilizer production primarily comes from nonrenewable sources and is generated through chemical synthesis reactions. These reactions produce intermediate products of broad commercial value for other industries and mineral salts in solid or liquid form (IFDC and UNIDO, 1979). The primary raw material for producing phosphate fertilizers is phosphate rock, a mineral extracted from the ground (Geissler et al., 2018). Phosphate or phosphate rock is treated with sulfuric acid to produce phosphoric acid, which is then concentrated or mixed with ammonia to create a variety of phosphate fertilizers (P2O5). It may also be treated with other inorganic acids (nitric or hydrochloric) or organic acids (citric) to generate other phospho-nitrogen compounds, such as MAP and DAP, and potassium salts to form complex NPK mixtures. Potassium fertilizers, conversely, come from treating mineral rocks in the soil and reusing ashes and organic waste. Through several chemical processes, the potash rock and these materials are converted into plant food, obtaining potassium chloride, sulfate, and nitrate salts (Fertilizers Europe, 2023).

Challenges in phosphorus plant availability

Plants absorb phosphorus in the orthophosphate (Pi) forms H2PO4– and HPO42–, found in soil solutions at deficient concentrations of 0.1–10 μM (Hinsinger, 2001). An optimal pH for absorption of Pi of 4.5 to 5.0 indicates a preferential uptake of H2PO4- by the plant over HPO42– (Raghothama, 1999). The soil solution P concentration gradient for plant cells exceeds 2000 times, with an average inorganic phosphate (Pi) concentration of 1 μM in the soil solution (Bieleski, 1973). This concentration is well below the Km of plant uptake. Therefore, although bound P is relatively abundant in many soils, it is largely unavailable for uptake. As such, P is frequently the most limiting element for plant growth and development. Crop yields, which are between 30 % and 40 % of the arable land in the world, are limited by the availability of P (Schachtman et al., 1998).

Although the total P content of soil generally ranges from 500 to 2000 ppm, the total bioavailable P, measured by soil extractors, maybe only a few ppm (Sanyal and DeDatta, 1991). Up to half of soil P can be organic, derived from plant residues and soil organisms, where the utilization of organic P by plants and microorganisms requires the mineralization (hydrolysis) of substrates by phosphatase enzymes that can be of plant or microbial origin. This increases phosphatase activity in response to P deficiency as part of P deficiency responses (Horst et al., 2001). In plants, this includes the release from roots of extracellular phosphatases that are considered necessary to capture and recycle organic P lost from roots or to allow greater access to soil organic P (Richardson et al., 2005). In response to P deficiency, increased phosphatase activity in the rhizosphere has been observed in many plant species. It is commonly reported to be higher in P-deficient soils (Richardson and Simpson, 2011).

Although P is an essential nutrient, plants only absorb a small fraction, estimated at 20 to 25 % of the P fertilizer applied to a crop. There has been a long-held view that any P residue is fixed in the soil and is unavailable for use by following crops (Johnston et al., 2014). Additionally, phosphorus is unavailable because it rapidly forms insoluble complexes with cations, particularly aluminum and iron, under acidic conditions. For example, since the 1980s, it has been documented that eroded, acidic soils in the tropics and subtropics are particularly prone to P deficiency (Sanchez and Uehara, 1980). This is where applying fertilizers containing P intervenes as the recommended treatment to improve the availability of P in the soil and stimulate crop yields (Vance et al., 2003).

However, applying phosphate fertilizers presents environmental challenges for both intensive and extensive agriculture in developed and developing countries. Because, in intensive agriculture, to obtain a corn yield of 6 to 9 t ha-1, an absorption of 30 to 50 kg P ha-1 is required (Ellington, 1999; Vance, 2001; Johnston, 2002), of which approximately two-thirds are removed in the harvested portion of the harvest. Small grains yielding 3 t ha-1 again absorb between 15 and 22 kg P ha-1 with a removal rate of 70 %. For example, soybeans absorb 20 to 25 kg of P ha-1, and 80 to 100 % is removed in the harvested portion (Johnston, 2002). However, as already mentioned, even with adequate P fertilization, only 20 % or less of the applied P is removed during the first year's growth due to soil retention (Russell, 1973).

Phosphate rock and apatite minerals as a phosphorus reserve

Reserves of mineral phosphorus in nature are found geologically in sedimentary rocks of apatite, which is the primary source of phosphorus and phosphate and is essential in manufacturing phosphoric acid and mineral fertilizers (Van Kauwenbergh, 2010). Some of them like carbonate apatite and igneous rocks fluoro‑chloro‑hydroxy-apatite formed by fire (Hughes and Rakovan, 2015). Apatite is part of a substitutional solid solution, in which atoms of approximately the same size replace the original atoms of the crystal lattice. The general composition of apatite is expressed as A(5XO4)3Zq, and various elements can be substituted for A, X, and Z (Kono et al., 2022). Hughes and Rakovar (2015) presented the diversity of the variations in the chemical composition of apatite. Pan and Fleet (2002), investigated minerals included in the apatite group and synthetic apatite and summarized their elemental substitutions (Fig. 1), including 53 elements, about half the 109 elements in the periodic table, that can be substituted in the apatite crystal structure. For example, in the apatite series, Ca5(PO4)3(F, OH, and Cl), the apices of the compositional triangle can be represented by F, OH, and Cl, respectively, making A = Fluorapatite, B = Hydroxylapatite, and C = Chlorapatite.” (Fig. 1). According to Kono et al., 2022, these are a group of mineral phosphates whose approximate chemical composition is Ca5(PO4)3 (F, Cl, OH). Depending on the anion that predominates in the second part of the formula, three species are considered: fluorapatite (Ca5(PO4)3 F), which is the main mineral of tooth enamel; chlorapatite (Ca5(PO4)3 Cl) and hydroxyapatite (Ca5(PO4)3 OH) the main mineral of bones. For instance, in the OH–F series, hydroxyapatite includes all combinations in the composition range of Ca10(PO4)6(OH)2 to Ca10(PO4)6 (OH, F)2. The color of the rock is variable, although colorless, white, yellow, and rarely brownish or greenish specimens predominate; they are also frequently found in hexagonal crystals (White and Dong, 2003).

Fig 1.

Fig 1

Open in a new tab

Periodic table of the elements that occur in apatite minerals and Diagrammatic representation of a complete ternary solid-solution series. a) The elements present in apatite supergroup minerals in the range of ppm to several tenths’ percent of total weight. The relevant elements are shown in red. This figure was prepared by Hughes and Rakovan (2015) based on the data from Pan and Fleet (2002). b) Diagrammatic representation of a complete ternary solid-solution series. A, B, and C represent the three compositional fields that merit a mineral name. Considering apatite as an example, the three vertices (A, B, and C) representing fluorapatite, hydroxyapatite, and chlorapatite, respectively. Then by the 50 % rule, in the OH-F system, the components of Ca10(PO4)6(OH)2 to Ca10(PO4)6(OH, F) are called hydroxyapatite (Kono et al. 2022).

Notably, 90 % of phosphate rock (PR) is used for food production: 82 % for fertilizers, 5 % for feed, and between 2 % and 3 % for food additives (Castro and Melgar, 2005). However, phosphorus resources are unevenly distributed globally: more than 95 % of P rock is found in 10 countries (Morocco and Western Sahara alone control 75 % of global reserves), and 6 % in China (Roy et al., 2022; Kiani, 2023). However, the accelerated flow of phosphate rock from the Earth's crust for fertilizer use has been both a blessing and a curse for food security and the environment, increasing crop yields while also leading to widespread water contamination and creating a precarious dependence of the world's food systems on a single source of phosphorus (Cordell and White, 2014).

The environmental cost of phosphorus mismanagement

It is worth mentioning that P, like nitrogen, is a pnictogenous element due to its electronic configuration in the outer layer, and this strongly affects its chemodynamic behavior. Unlike N, P5+ oxides in the highest oxidation state tend to be highly insoluble with metal ions (especially Mg2+ and Ca2+), which are the most abundant in the Earth's crust and when combined with trivalent ions. Such as Fe3+and Al3+. The forms of inorganic P include precipitated P-containing minerals, defined as minerals that contain P as a structural element, such as apatites, strange, and variscite, which are very stable, and their solubility depends on the pH of the soil (Jusino- Maldonado et al., 2022).

Meanwhile, the secondary forms are adsorbed or bound P, such as minerals that absorb P, mainly Al, Ca, and Fe (El Bamiki et al., 2021). This is the fate of many phosphate fertilizers, including diammonium phosphate, mono ammonium phosphate, triple superphosphate, and single superphosphate (amounting to about 16.5 ± 3 Mt year-1 P), which are marketed worldwide and are applied to agricultural fields and pastures around the world (Alewell et al.,2020). However, plant roots absorb only 15–30 % of the annually applied phosphorus in fertilizers (in addition to residual soil phosphorus), which subsequently dissolves into the soil solution (Zhao et al., 2021).

That is why phosphorus in soil exists in different chemical forms, whether organic or inorganic (Pi). In addition to the readily available P fraction that phosphate fertilizers can significantly provide, the activities of both roots and associated microorganisms also contribute to improving P availability in the rhizosphere soil (Richardson and Simpson, 2011). However, these advantages are coupled at a significant cost. Mobilizing phosphate rock into the environment much faster alters the global phosphorus cycle by mobilizing four times the natural phosphorus level from phosphate rock to the environment (Tian et al., 2021).

Phosphorus enters the livestock sector through feed, forage, supplements, fertilized pastures, or natural grasslands. Once phosphorus is consumed, it leaves the world's feedlots, pastures, and grasslands as animal products, and the rest ends up in manure and eroded soils (Zhao et al., 2021). Manure alone is estimated to contain about 16 ± 1 Mt year-1 of P from the world's 63 billion livestock. Half of this is productively reused in agricultural or grassland soils, while the other half is estimated to be lost to non-agricultural soils or water. Approximately 11 Mt of P is absorbed by crops and grasslands each year, while an estimated 12 Mt of P is added to soil reserves yearly. About 5 ± 3 Mt year-1 of soil P is exported through wind and water erosion from fields to water bodies and non-agricultural soils (Alewell et al., 2020). Other, more conservative estimates speak of a loss of up to 4–6 Mt P year-1 reaching the soil to the oceans (Filippeli, 2008).

Some authors estimate that human intervention in the global phosphorus cycle has mobilized an additional 22 Mt year-1 of P to enter the ocean, contributing to 50 % of its loss beyond the natural cycle (Alewell et al., 2020). This intervention leads to excess nutrients in freshwater and oceans, causing eutrophication. This process can lead to excessive growth of toxic algal blooms, with severe consequences for aquatic ecosystems, water quality, and recreation (McMahon and Read, 2013). The adverse effects of eutrophication cannot be overstated, making it a critical issue to address.

Sustainable opportunities for phosphorus management

A deficiency in phosphorus can lead to reduced crop yields, which poses a significant threat to food security. It is estimated that by 2050, more than 5.7 billion people could face phosphorus scarcity (White et al., 2010). Addressing this issue requires efficient cultivation and storage practices, as well as maintaining a consistent supply of organic phosphorus from soil macromolecules. The historical addition of phosphate to soils through mining activities during the 19th and 20th centuries raises environmental concerns, including soil degradation and water pollution (Elrys et al., 2021; Nedelciu et al., 2020). Proper management of phosphorus resources is crucial to minimizing these environmental risks while ensuring sustainable agricultural productivity.

However, organic matter contains about 80 % of total soil P and is the important reservoir of soil P, although it is often primarily unavailable to plants. A similar situation prevails in the rhizosphere, which is the proximity of plant roots (Senesi and Loffredo, 2018). However, one of the many exciting microorganisms living in the rhizosphere is a soil bacterium called Pseudomonas. Like many other representatives of this genus, Pseudomonas fluorescens are motile and possess a polar flagellum (Yanes and Bajsa, 2016). These organisms contain the enzyme phosphatase, responsible for the microbial solubilization of inorganic P. These bacteria are PSMs, and because of their rhizosphere location in soil, Pseudomonas species are candidates for exploitation in sustainable agriculture (Kögel-Knabner and Amelung, 2021; Witzgall et al., 2021).

Microbial phosphorus solubilization

To increase the agronomic efficiency of PR, the use of agriculturally essential microorganisms involved in the P cycle is a promising biotechnological strategy that has gained global interest in recent decades. In early studies, PSMs were defined as microbes that transform insoluble Pi and Po into soluble P forms and regulate the biogeochemical cycle of P in agroecosystems (Halder and Chakrabartty, 1993; Sperber, 1957). Among the heterogeneously distributed soil microflora, a large number of heterotrophic and autotrophic microorganisms are commonly found, including phosphate-solubilizing bacteria (PSB), phosphate-solubilizing fungi (PSF), phosphate-solubilizing actinomycetes (PSA), and cyanobacteria (Turan et al., 2006; Zaidi et al., 2010; Maharana et al., 2021). PSBs, such as Bacillus sp., Pseudomonas sp., Rhizobium sp., and Escherichia sp., among many others, form the largest microbial communities with P solubilization capacity in soil (Tian et al., 2021).

Microorganisms solubilize phosphorus through several mechanisms, including organic acids, enzyme production, siderophore synthesis, and microbial respiration. Organic acids help dissolve phosphorus by acidifying the rhizosphere, while enzymes like phosphatases convert organic phosphorus into soluble forms. Siderophores chelate metal cations, aiding phosphorus release and enhancing efficiency (Table 1). Acid phosphatases are more effective in acids soils, while alkaline phosphatases function optimally in basic soil conditions.

Table 1.

Biotechnological strategies and applications of microbial phosphorus solubilization.

Organism Mechanism Application Reference
Rhizobium sp. Production of 2-keto gluconic acid Solubilization of hydroxyapatite Halder et al. (1993)
Aspergillus niger and Penicillium sp. Phytases and acid phosphatases. Rock phosphate solubilization Saber et al. (2009)
Aspergillus niger Production of oxalic acid Rock phosphate solubilization Schneider et al. (2010)
Bacillus sp. Gluconic, lactic, acetic, succinic and propionic acid. Solubilization of ash, bones, fish bones, and phosphate rock. Saeid et al. (2018)
Aspergillus niger
Trichoderma reesei 		Phytases and phosphatases Chemical industry, biofuels, and animal nutrition. Ribeiro Corrêa and Fernandes de Araújo (2020)
Burkholderia sp., and Rahnella sp. Solubilization by organic acids. Endophytes of
Populus trichocarpa 		Varga et al. (2020)
Burkholderia sp., and
Paraburkholderia sp.		 Production of organic acids and siderophores. Plant growth promotion in Zea mays L. Barrera-Galicia et al. (2021)
Pleurotus ostreatus Tartaric, malic, citric, lactic, and succinic acid. Rock phosphate solubilization Maharana et al. (2021)
Penicillium sp. pH reduction by organic acids. Phosphate
chelation of heavy metals		 Eigbike and Salihu (2023)
Open in a new tab

The biological solubilization process of PR is significantly influenced by the microbial production of organic acids, which play a crucial role in chelating the cations (mainly calcium) bound to the phosphate (Fig 1). Several studies have shed light on the efficiency of these compounds, with oxalic acid being the most effective, followed by citric, malic, itaconic, and gluconic acids. For instance, using the phosphate rock called apatite [Ca5(PO4)3(OH, F, Cl)], for every mmol of oxalic acid, 21 mg of phosphorus were released, while sulfuric acid solubilized 14 mg of phosphorus (de Oliveira Mendes et al., 2020).

Schneider et al. (2010) reported that after the solubilization of PR by Aspergillus niger, all oxalic acid produced precipitated as calcium oxalate crystals. Therefore, the formation of calcium oxalate contributes to the solubilization of apatite by removing Ca2+ from the solution and by ligand exchange reactions at the mineral surface (Kaleeswari and Subramanian, 2001; Robinson et al., 1992; Stumm, 1986; Welch et al., 2002).

Microbial respiration and the release of CO2 can contribute to phosphorus solubilization. The increase in CO2 concentration in the rhizosphere leads to the formation of carbonic acid, which further contributes to the acidification of the soil and promotes the dissolution of calcium phosphate (Rawat et al., 2021).

Many experimental studies have proved synergies can occur when combining PSB and PR, likely leading to cost-effective P-based microbial inoculants directly applicable to acidic or alkaline soils (Richardson and Simpson, 2011). For example, the dual application of PR and PSB (such as Azotobacter, Azosporillum, Rhizobium, and Klebsiella) significantly improved the P nutrition of both cereal and legume plants (Tomer et al., 2016). Moreover, the extracellular exudation of enzymes into the rhizosphere, either by roots or associated microorganisms, are additional mechanisms that contribute significantly to improving P availability (Rawat et al., 2021), with acid phosphatases being the most P-hydrolyzing enzymes, abundantly produced under low P conditions (Vance et al., 2003).

This comprehensive set of mechanisms highlights how microbial activity is critical in making phosphorus more available to plants, thus supporting sustainable nutrient management in agriculture.

Microbial enzymes for phosphorus solubilization

Phytase enzymes (myoinositol hexakisphosphate phosphohydrolases) are phosphatases that hydrolyze phytic acid (phytates), preferably to Myo-inositol and six inorganic phosphors. Still, releasing mono, di, tri, tetra, or penta phosphate intermediates is possible when hydrolysis occurs (Ribeiro Corrêa and Fernandes de Araújo, 2020). Phytases can be classified based on the attack on the carbon molecule present in phytic acid, pH optima, or catalysis and structural information (Singh et al., 2020). Based on catalysis and structural information, Mullaney and Ullah, in 2003, classified phytases into histidine, acidic phosphatases, purple acid phosphatases, and β-helix-propeller phytases (BPPs alkaline phytases) according to their catalytic domains. Subsequently, Chu et al. (2004) reported isolating and characterizing a cysteine phytase from a bacteria found in the bovine rumen. The dependence of all living organisms on Pi has led nature to develop many types of catalytic mechanisms to split phytic acid into Pi (Mullaney, 2007). Generally, phytases are grouped into four different groups phytases and three classes, namely histidine acid phosphatases, cysteine phytase, and β-propeller phytase, have been reported as being of microbial origin (Singh et al., 2020). Animals, plants, and microorganisms ubiquitously produce these enzymes and generally exhibit optimal activity at pH and temperature of 4.5 to 6.0 and 45 to 60 °C, respectively, with an acid isoelectric point, the molecular weight of around 40 to 70 kDa and monomeric state (Ribeiro Corrêa and Fernandes de Araújo, 2020).

Phytates are abundantly present in the soil in the form of organic P. However, they are relatively unavailable to plants because plants have no phytase activity in their root systems. Therefore, the ability of plants to uptake phytate-P from soils would be improved by direct supplementation of a phytase enzyme or by inoculation with a microbial strain that can release phytase (Singh et al., 2020).

For example, phytase activity was recently recorded in two bacterial enzymes of the metallo-β-lactamase family, expanding the phosphatase activity to other proteins (Castillo Villamizar et al., 2019). PAHs are recognized as “fungal phytases,” such as those present in Aspergillus niger. However, they are also present in bacteria, yeasts, and plants (Ribeiro Corrêa and Fernandes de Araújo, 2020). Most research has focused on the application of phytases in animal nutrition. Phytases represent 60 % of the feed enzyme market, equivalent to $350 million annually. Moreover, about 70 % of feeds contain phytase as an additive (Gontia et al., 2012).

While phytase is widely recognized for its ability to break down phytic acid, other enzymes such as phosphatases, carbon-phosphorus lyases, and d-glycerophosphatases also significantly contribute to phosphorus cycling. Phosphatases catalyze the hydrolysis of organic phosphorus compounds. Phosphatases are classified into two main categories based on their optimal pH: acid and alkaline phosphatases. Acid phosphatases are commonly found in fungi and certain bacteria and are produced in the phloem, cortex, epidermis, and roots of plants. In contrast, alkaline phosphatases are prevalent in a variety of microbial species and are active in basic soil with a pH > 7 (Campdelacreu Rocabruna et al., 2024). Carbon-phosphorus lyases cleave the strong carbon-phosphorus bonds in organophosphonates. This enzyme system is especially relevant in agricultural soils with high organophosphonate content, as it enables microorganisms to access phosphorus from these compounds (Silva et al., 2023). d-glycerophosphatase assists in the mineralization of glycerophosphate, which is a low molecular weight form of organic phosphorus (Turner et al., 2005).

These enzymatic activities collectively enhance the availability of phosphorus for plant growth, reduce the reliance on chemical fertilizers, and promote sustainable agricultural practices, highlighting the importance of microbial enzymes in nutrient management and soil fertility.

Development of inoculants for sustainable use of phosphorus

Ecological consideration should be taken as a starting point to create innovative fertilization strategies in which both environmental and biological processes (such as, specific nutrient interactions in the rhizosphere and plants, soil and plant microbiomes, etc.), and technologies can be combined, exploited through concerted research and development efforts to achieve the goal of sustainable agricultural production (Fig. 2). Solubilization of phosphate rock by microorganisms is an environmentally sustainable alternative to chemical processing for the production of phosphate fertilizers (Rawat et al., 2021). In some studies, it has been seen that the interaction of PSMs (Pseudomonas, Mycobacterium, Bacillus, Pantoea, Rhizobia, and Burkholderia) and phosphate fertilizers improved wheat grain yield (22 %) and phosphorus absorption (26 %) by the time that reduced the fertilizer contribution by 30 % (from 120 to 90 kg P2O5 ha−1). Moreover, these microbial inoculants are safe and non-toxic to the environment.

Fig. 2.

Fig 2

Open in a new tab

Development process of microbial inoculants for the use of phosphate rock as a sustainable agricultural production strategy. The red arrows indicate the steps to follow; however, they are only representative since the methodologies used vary depending on the available resources and the advancement of microbiological characterization techniques. The solubility of phosphorus carried out by soil microbes may be mediated by the release of organic acids, production of enzymes, or acidification mechanisms (release of protons) that facilitate the absorption of phosphate available (HPO42–, PO43-, H2PO4–) for plants (Raymond et al., 2021). In this work, we also propose evaluating and measuring phosphorus solubility based on microbial activity and considering the biosafety of the inoculant.

Batch solids addition achieves an effective solubilization activation strategy that is very promising compared to the results reported elsewhere for similar conventional and PR processes (igneous origin). Saber et al. (2009) cultivated A. niger under SmC using a similar igneous PR (fluorapatite rock from Giza, Egypt) and obtained 99.7 mg L−1 soluble phosphorus after 216 h Under similar conditions, Schneider et al., 2010 obtained 281 mg l-1 of soluble phosphorus after 192 h of cultivation using hydroxyapatite rock from Catalão, Brazil. De Oliveira Mendes et al., 2020, also grew A. niger under SmC using Araxá rock from Brazil, and obtained 74.4 mg l-1 of soluble phosphorus after 144 h In this work, the maximum soluble P concentration obtained was approximately 350 mg L−1 after a processing time of only 120 h (Klaic et al., 2021).

In addition to the use of PSMs for nutritional purposes, some of these microorganisms have been described to promote plant growth; some of the most interesting are those belonging to Burkholderia sensu lato, which are rhizosphere bacteria of corn, which also have an effect of biocontrol, mediating the suppression of rot caused by Fusarium spp., in the roots of corn (Barrera-Galicia et al., 2021). Among the most exciting strains, those of the Paraburkolderia genus stand out, such as P. kisternboschensis, P. graminis, and P. rhynchosiae with phosphorus solubilization activities (399, 415, and 475 mg l-1 of P, respectively), these bacteria are capable of growing using an insoluble phosphate source (Fig. 3). Likewise, some other activities have been determined, such as nitrogen fixation through the acetylene reduction test, production of siderophores, and generation of exopolysaccharides (Barrera-Galicia, 2023). Plant Growth Promoting Microorganisms (PGPMs) change the pH of the soil to solubilize inorganic phosphates. In alkaline soils, pH is reduced due to the excretion of organic acids, such as gluconate, citrate, lactate, and succinate, solubilizing Ca3(PO4)2. Moreover, in acidic soils, MPCV increases the production of protons during the assimilation of ammonium (NH4+), solubilizing AlPO4 and FePO4 (Martínez-Viveros et al., 2010).

Fig. 3.

Fig 3

Open in a new tab

Technique for the microbial solubilization activity of phosphoric rock. The red arrows describe the research process implemented in our laboratory to develop a methodology for evaluating, characterizing, and measuring microbial solubilization activity. In this example, the phosphorus source used is commercial phosphate rock; however, other sources of phosphorus can be implemented. Phosphorus includes dicalcium, tricalcium phosphate, magnesium phosphate, apatite, and other sources of insoluble phosphorus. Also, organic and inorganic acids are used to quantify the soluble phosphorus of different arrays.

Carrier materials play a vital role in the effectiveness of the bacterial formulation. The main properties of a suitable carrier are (i) non-toxicity to microbes, (ii) good exchange surface, (iii) ease of both sterilization and processing, (iv) availability in large quantities, renewable and economical, and (v) non-toxic to plants, human health, and the environment (Reddy, 2014).

Liquid bioformulations offer numerous advantages over traditional solid bioformulations, including extended shelf life, higher microbial viability, reduced risk of contamination, and enhanced field performance (Yafetto, 2022). These benefits have driven a surge in interest from companies worldwide, positioning liquid microbial inoculants as the next generation of sustainable agricultural inputs. In countries like Japan and the United States, companies are actively producing and utilizing microbial inoculants with Rhizobium spp. as inoculants for a variety of crops, including lentils, soybeans, corn, sorghum, sugar beets, wheat, and canola (Yafetto et al., 2023).

Since the early 2000s, research interest in these microorganisms has significantly grown, reflecting their role in sustainable agriculture and mitigating phosphorus scarcity. Among the leading contributors to research output, India stands out with 542 published papers, followed by China (336), Brazil (225), Pakistan (217), and the United States (158). Collectively, these five countries account for 52.6 % of the total research publications, highlighting their major contributions to this field, likely driven by their vast agricultural sectors and significant demand for phosphorus-based fertilizers (Ramos Cabrera et al., 2024).

Recent advances in microbial engineering for phosphorus solubilization

Microbial engineering has emerged as a promising field to enhance phosphorus solubilization, facilitating a transition to sustainable agricultural practices. Recent advancements have primarily focused on genetic modifications that improve the efficiency of microorganisms in mobilizing phosphorus from insoluble sources. These engineered microorganisms are crucial for increasing nutrient availability and boosting crop productivity. One of the most prominent advances has been engineering microbial strains, particularly those of Pseudomonas, Bacillus, and Rhizobium, to overproduce organic acids such as citric and gluconic acids. These acids play a critical role in solubilizing calcium-bound phosphates in the soil. Genetic modification has been employed to enhance metabolic pathways responsible for organic acid production, increasing the overall efficiency of phosphorus release. These engineered strains demonstrate a higher capacity for making phosphorus bioavailable to plants under various soil conditions (Ke et al., 2021; Singh et al., 2024; Xu et al., 2020).

The application of CRISPR-Cas9 technology has allowed for precise editing of genes involved in phosphorus solubilization. Researchers have targeted specific genes that regulate phosphate transport systems and organic acid production. By fine-tuning these genes, engineered bacteria can produce more effective enzymes and acids, optimizing phosphorus solubilization without negatively impacting other microbial functions (Fazeli-Nasab and Rahmani, 2021; Malik et al., 2024; Singh et al., 2024). This approach has enabled the creation of microbial strains tailored to different soil types and agricultural needs.

Advances in synthetic biology have facilitated the design of microbial consortia where different strains are engineered to cooperate synergistically, enhancing phosphorus solubilization efficiency. For example, recent studies have successfully engineered a straw-degrading bacterium that solubilizes phosphorus simultaneously. Such microbial consortia leverage complementary mechanisms—including acid production, enzyme secretion, and phosphorus uptake—creating a multifaceted approach to phosphorus bioavailability (Che et al., 2024; El Maaloum et al., 2020; Emami et al., 2020). Beyond improving organic acid production, enzyme engineering has also played a vital role in recent advances. Phosphatases, phytases, and other enzymes key to phosphorus mineralization have been genetically enhanced to be more stable under various environmental conditions, including extreme pH and temperature. When expressed by soil microorganisms, these engineered enzymes significantly increase the phosphorus solubilization rate, thereby improving plant nutrient uptake (Li et al., 2024; Timofeeva et al., 2022). Another recent development involves modifying quorum sensing mechanisms in phosphorus-solubilizing microorganisms (PSMs). Quorum sensing, a process by which bacteria communicate based on population density, is crucial for coordinating enzyme secretion and organic acid production. Researchers have successfully engineered PSMs to either overexpress or inhibit specific quorum sensing pathways, ensuring a more controlled and efficient phosphorus solubilization process (Lucero et al., 2023; Zhang et al., 2023).

Conclusion

Phosphorus is indispensable for plant nutrition and agricultural productivity, yet its availability in the soil presents a significant challenge due to its tendency to bind with other elements and form insoluble compounds. Conventional practices, such as the excessive application of chemical phosphorus fertilizers, have led to severe environmental consequences, including water pollution and soil degradation. The global dependency on finite phosphate rock reserves further exacerbates the need for sustainable alternatives in phosphorus management.

Microbial phosphorus solubilization offers a promising solution to these challenges. PSMs and their enzymes can mobilize phosphorus from insoluble sources through various mechanisms, such as rhizosphere acidification and phosphatase excretion. This approach supports the development of microbial inoculants for in situ application, enhancing phosphorus uptake by plants. Advances in microbial inoculant development can contribute to sustainable and efficient phosphorus use in agriculture, reducing dependence on chemical fertilizers and minimizing environmental impact.

Advanced sequencing techniques, such as metagenomics and metatranscriptomics, can reveal the diversity of microbial communities capable of phosphorus solubilization and their gene expression under different soil and environmental conditions. This approach would provide insights into understanding the specific genes and molecular pathways involved in phosphorus solubilization, paving the way for targeted interventions (Hu et al., 2023). Future research can also focus on genetically engineering PSMs to enhance their efficiency in solubilizing various insoluble forms of phosphorus (Rawat et al., 2021).

The integration of microbial solutions into phosphorus management offers a pathway to more sustainable agricultural systems, promoting nutrient cycling, soil health, and long-term productivity. However, challenges remain in scaling up microbial technologies and ensuring their effectiveness across diverse agroecosystems. Future research should focus on optimizing microbial inoculants, understanding their interactions in different soil environments, and developing strategies to maximize their potential in sustainability agriculture.

Funding

There is no funding agency available at the present time.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

CRediT authorship contribution statement

José Abraham García-Berumen: Conceptualization, Writing – original draft, writing – review & editing. Juan Armando Flores de la Torre: Writing – original draft, writing – review & editing. Sergio de los Santos-Villalobos: Writing – original draft, writing – review & editing. Alejandro Espinoza-Canales: Writing – original draft, writing – review. Francisco G. Echavarría-Cháirez: Writing – original draft, writing – review. Héctor Gutiérrez-Bañuelos: Conceptualization, Writing – original draft, writing – review & final editing.

Declaration of competing interest

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

Acknowledgements

The author is thankful to CONAHCYT (National Council of Humanities Sciences and Technologies) from the Mexican government for the scholarship to José Abraham García-Berumen (No. CVU: 564458, Application number reference: 651c45209f7f66514918c884), also, to the “Doctorado en Ciencias Agropecuarias (Ph. D. in Agricultural Sciences)” program of the Autonomous University of Zacatecas, Mexico (Reference 005870).

Data availability

No data was used for the research described in the article.

References

  1. Alewell C., Ringeval B., Ballabio C., Robinson D.A., Panagos P., Borrelli P. Global phosphorus shortage will be aggravated by soil erosion. Nat. Commun. 2020;11(1):4546. doi: 10.1038/s41467-020-18326-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Asimov I. Doubleday; New York: 1974. Asimov On Chemistry. [Google Scholar]
  3. Barrera Galicia G.C. Supresión de la pudrición de la raíz del maíz (Fusarium spp.) mediada por las actividades metabólicas de Burkholderia sensu lato. (Tesis doctoral) CINVESTAV Unidad Irapuato. 2023 [Google Scholar]
  4. Barrera-Galicia G.C., Peniche-Pavía H.A., Peña-Cabriales J.J., Covarrubias S.A., Vera-Núñez J.A., Délano-Frier J.P. Metabolic footprints of Burkholderia sensu lato rhizosphere bacteria active against maize Fusarium pathogens. Microorganisms. 2021;9(10):2061. doi: 10.3390/microorganisms9102061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bieleski R.L. Phosphate pools, phosphate transport, and phosphate availability. Annu. Rev. Plant Physiol. 1973;24:225–252. [Google Scholar]
  6. Campdelacreu Rocabruna P., Domene X., Preece C., Peñuelas J. Relationship among soil biophysicochemical properties, agricultural practices and climate factors influencing soil phosphatase activity in agricultural land. Agriculture. 2024;14(2):288. doi: 10.3390/agriculture14020288. [DOI] [Google Scholar]
  7. Castillo Villamizar G.A., Funkner K., Nacke H., Foerster K., Daniel R. Functional metagenomics reveals a new catalytic domain, the metallo-β-lactamase superfamily domain, associated with phytase activity. mSphere. 2019;4 doi: 10.1128/msphere.00167-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Castro L., Melgar R. Rocas Fosfóricas. Capítulo Introductorio. Miner. para la Agric. en Latinoamérica. 2005:39–61. [Google Scholar]
  9. Che S., Xu Y., Qin X., Tian S., Wang J., Zhou X., Cao Z., Wang D., Wu M., Wu Z., Yang M., Wu L., Yang X. Building microbial consortia to enhance straw degradation, phosphorus solubilization, and soil fertility for rice growth. Microb. Cell Fact. 2024;23(1):232. doi: 10.1186/s12934-024-02503-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chu H.-M., Guo R.-T., Lin T.-W., Chou C.-C., Shr H.-L., Lai H.-L., Tang T.-Y., Cheng K.-J., Selinger B.L., Wang A-H.J. Structures of Selenomonas ruminantium phytase in complex with persulfated phytate: DSP phytase fold and mechanism for sequential substrate hydrolysis. Structure. 2004;12:2015–2024. doi: 10.1016/j.str.2004.08.010. [DOI] [PubMed] [Google Scholar]
  11. Cordell D., White S. Peak phosphorus: clarifying the key issues of a vigorous debate about long-term phosphorus security. Sustainability. 2011;3(10):2027–2049. doi: 10.3390/su3102027. [DOI] [Google Scholar]
  12. Cordell D., White S. Life's bottleneck: sustaining the world's phosphorus for a food secure future. Annu. Rev. Environ. Resour. 2014;39:161–188. [Google Scholar]
  13. de Oliveira Mendes G., Murta H.M., Valadares R.V., da Silveira W.B., da Silva I.R., Costa M.D. Oxalic acid is more efficient than sulfuric acid for rock phosphate solubilization. Miner. Eng. 2020;155 doi: 10.1016/j.mineng.2020.106458. [DOI] [Google Scholar]
  14. Dey G., Banerjee P., Sharma R.K., Maity J.P., Etesami H., Shaw A.K., Huang Y.-H., Huang H.-B., Chen C.Y. Management of phosphorus in salinity-stressed agriculture for sustainable crop production by salt-tolerant phosphate-solubilizing bacteria— a review. Agronomy. 2021;11(8):1552. doi: 10.3390/agronomy11081552. [DOI] [Google Scholar]
  15. Dissanayaka D.M.S.B., Ghahremani M., Siebers M., Wasaki J., Plaxton W.C. Recent insights into the metabolic adaptations of phosphorus-deprived plants. J. Exp. Bot. 2021;72(2):199–223. doi: 10.1093/jxb/eraa482. [DOI] [PubMed] [Google Scholar]
  16. Eigbike C.O., Salihu A.K. Immobilization of heavy metals in contaminated soil using calcium phosphate amendment and phosphate-solubilizing fungi (Penicillium sp) in Benin City, Edo state, Nigeria. J. Appl. Sci. Environ. Manag. 2023;27(2):355–360. doi: 10.4314/jasem.v27i2.25. [DOI] [Google Scholar]
  17. El Bamiki R., Raji O., Ouabid M., Elghali A., Khadiri Yazami O., Bodinier J.L. Phosphate rocks: a review of sedimentary and igneous occurrences in Morocco. Minerals. 2021;11(10):1137. doi: 10.3390/min11101137. [DOI] [Google Scholar]
  18. El Maaloum S., Elabed A., Alaoui-Talibi Z.E., Meddich A., Filali-Maltouf A., Douira A., Ibnsouda-Koraichi S., Amir S., El Modafar C. Effect of arbuscular mycorrhizal fungi and phosphate-solubilizing bacteria consortia associated with phospho-compost on phosphorus solubilization and growth of tomato seedlings (Solanum lycopersicum L.) Commun Soil Sci. Plant Anal. 2020;51(5):622–634. doi: 10.1080/00103624.2020.1729376. [DOI] [Google Scholar]
  19. Ellington C.P. In: Phosphorus for Agriculture: a Situation Analysis. Ellington CP, editor. Potash/Phosphate Institute; Norcross, GA, USA: 1999. Crop yield responses to phosphorus; pp. 25–41. [Google Scholar]
  20. Elrys A.S., Desoky E.S.M., Ali A., Zhang J.B., Cai Z.C., Cheng Y. Sub-Saharan Africa's food nitrogen and phosphorus footprints: a scenario analysis for 2050. Sci. Total Environ. 2021;752 doi: 10.1016/j.scitotenv.2020.141964. [DOI] [PubMed] [Google Scholar]
  21. Emami S., Alikhani H.A., Pourbabaee A.A., Etesami H., Motasharezadeh B., Sarmadian F. Consortium of endophyte and rhizosphere phosphate solubilizing bacteria improves phosphorous use efficiency in wheat cultivars in phosphorus deficient soils. Rhizosphere. 2020;14 doi: 10.1016/j.rhisph.2020.100196. [DOI] [Google Scholar]
  22. FAO Los fertilizantes y su uso. Fundamento de la necesidad de fertilizantes. Cap. 2022;2:1–5. págs. [Google Scholar]
  23. FAO, 2023. Objetivos de desarrollo sostenible dentro del marco estratégico de la para 2022–2031. https://www.fao.org/office-of-sustainable-development-goals/es (Accesed 2.5.23).
  24. Fazeli-Nasab B., Rahmani A.F. Springer; Singapore: 2021. Microbial genes, Enzymes, and Metabolites: To improve Rhizosphere and Plant Health management. Microbiological Activity for Soil and Plant Health Management; pp. 459–506. [DOI] [Google Scholar]
  25. Fertilizers Europe, 2023. https://www.fertilizerseurope.com/AnnualOverview/fertilizers-europe.html (Accesed 4.7.23).
  26. Filippelli G.M. The global phosphorus cycle: past, present, and future. Elements. 2008;4(2):89–95. [Google Scholar]
  27. Geissler B., Hermann L., Mew M.C., Steiner G. Striving toward a circular economy for phosphorus: the role of phosphate rock mining. Minerals. 2018;8(9):395. [Google Scholar]
  28. Gontia I., Tantwai K., Singh Rajput L.P., Tiwari S. Transgenic plants expressing phytase gene of microbial origin and their prospective application as feed. Food Technol. Biotechnol. 2012;50(1):3–10. [Google Scholar]
  29. Halder A.K., Chakrabartty P.K. Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol. 1993;38:325–330. [Google Scholar]
  30. Hinsinger P. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil. 2001;237:173–195. [Google Scholar]
  31. Horst W.J., Kamh M., Jibrin J.M., Chude V.A. Agronomic measures for increasing P availability to crops. Plant Soil. 2001;237:211–233. [Google Scholar]
  32. Hu X., Gu H., Liu J., Wei D., Zhu P., Cui X.A., Zhou B., Chen X., Jin J., Liu X., Wang G. Metagenomic strategies uncover the soil bioavailable phosphorus improved by organic fertilization in Mollisols. Agric. Ecosyst. Environ. 2023;349 doi: 10.1016/j.agee.2023.108462. [DOI] [Google Scholar]
  33. Hughes J.M., Rakovan J.F. Structurally robust, chemically diverse: apatite and apatite supergroup minerals. Elements. 2015;11(3):165–170. doi: 10.2113/gselements.11.3.165. [DOI] [Google Scholar]
  34. IFDC (International Fertilizer Development Center) and UNIDO (United Nations Industrial Development Organization)., 1979. Fertilizer Manual. Published by Kluwer Academic Publishers.
  35. John D.A., Babu G.R. Lessons from the aftermaths of green revolution on food system and health. Front. Sustain. Food Syst. 2021;5 doi: 10.3389/fsufs.2021.644559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Johnston A.M. Nutrient removal as a soil fertility planning tool. Fertilization Facts. 2002 http://www.ppi-ppic.org [Google Scholar]
  37. Johnston A.E., Poulton P.R., Fixen P.E., Curtin D. Phosphorus: its efficient use in agriculture. Adv. Agron. 2014;123:177–228. doi: 10.1016/B978-0-12-420225-2.00005-4. [DOI] [Google Scholar]
  38. Jusino-Maldonado M., Rianço-Silva R., Mondal J.A., Pasek M., Laneuville M., Cleaves H.J. A global network model of abiotic phosphorus cycling on Earth through time. Sci. Rep. 2022;12(1):9348. doi: 10.1038/s41598-022-12994-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kaleeswari R.K., Subramanian S. Chemical reactivity of phosphate rocks a review. Agric. Rev. 2001;22:121–126. [Google Scholar]
  40. Kiani M. University of Helsinki; 2023. Closing the Phosphorus Cycle by Recycling Lake Sediments in Agriculture. Doctoral thesis. Department of Agriculture Sciences. Faculty of Agriculture and Forestry. Doctoral Programme in Sustainable Use of Renewable Natural Resources. [Google Scholar]
  41. Klaic R., Gava Junior M., Florencio C., Ribeiro C., Farinas C.S. Biological solubilization of phosphate rock by solid-state cultivation to produce eco-friendly fertilizers. Pesquisa Agropecuária Brasileira. 2021;56 doi: 10.1590/S1678-3921.pab2021.v56.01441. [DOI] [Google Scholar]
  42. Ke J., Wang B., Yoshikuni Y. Microbiome engineering: synthetic biology of plant-associated microbiomes in sustainable agriculture. Trends Biotechnol. 2021;39(3):244–261. doi: 10.1016/j.tibtech.2020.07.008. [DOI] [PubMed] [Google Scholar]
  43. Kögel-Knabner I., Amelung W. Soil organic matter in major pedogenic soil groups. Geoderma. 2021 doi: 10.1016/j.geoderma.2020.114785. [DOI] [Google Scholar]
  44. Kono T., Sakae T., Nakada H., Kaneda T., Okada H. Confusion between carbonate apatite and biological apatite (Carbonated Hydroxyapatite) in bone and teeth. Minerals. 2022;12:170. doi: 10.3390/min12020170. [DOI] [Google Scholar]
  45. Kumar S., Mohapatra T. Dynamics of DNA methylation and its functions in plant growth and development. Front. Plant Sci. 2021;12 doi: 10.3389/fpls.2021.596236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Li X., Tian J., Chen X., Liao H. Bioengineering and management for efficient and sustainable utilization of phosphorus in crops. Curr. Opin. Biotechnol. 2024;90 doi: 10.1016/j.copbio.2024.103180. [DOI] [PubMed] [Google Scholar]
  47. Liebig J. Friedrich Vieweg; Braunschweig, Ger: 1840. Die Organische Chemie in Ihrer Anwendung auf Agricultur und Physiologie [Organic chemistry in Its Applications to Agriculture and Physiology] [Google Scholar]
  48. Liu D. Root developmental responses to phosphorus nutrition. J. Integr. Plant Biol. 2021;63(6):1065–1090. doi: 10.1111/jipb.13090%3c/bib. [DOI] [PubMed] [Google Scholar]
  49. Lucero C.T., Lorda G.S., Halliday N., Ambrosino M.L., Cámara M., Taurian T. Impact of quorum sensing from native peanut phosphate solubilizing Serratia sp. S119 strain on interactions with agronomically important crops. Symbiosis. 2023;89(1):107–121. doi: 10.1007/s13199-022-00893-6%3c/bib. [DOI] [Google Scholar]
  50. Maharana R., Basu A., Dhal N.K., Adak T. Biosolubilization of rock phosphate by Pleurotus ostreatus with brewery sludge and its effect on the growth of maize (Zea mays L.) J. Plant Nutr. 2021;44(3):395–410. doi: 10.1080/01904167.2020.1822397. [DOI] [Google Scholar]
  51. Malik N.U.A., Khalid A.R., Gul A., Munir F., Haider G., Bhatti M.F. Targeted Genome Engineering Via CRISPR/Cas9 in Plants. Academic Press; 2024. CRISPR-Cas9-mediated genome editing in fungi: current scenario and future implications in agriculture, health, and industry; pp. 35–62. [DOI] [Google Scholar]
  52. Martínez-Viveros O., Jorquera M.A., Crowley D.E., Gajardo G., Mora M.L. Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J. Soil Sci. Plant Nutr. 2010;10:293–319. doi: 10.4067/S0718-95162010000100006. [DOI] [Google Scholar]
  53. McMahon K.D., Read E.K. Microbial contributions to phosphorus cycling in eutrophic lakes and wastewater. Annu. Rev. Microbiol. 2013;67:199–219. doi: 10.1146/annurev-micro-092412-155713. [DOI] [PubMed] [Google Scholar]
  54. Mullaney E.J. In: Inositol phosphates: Linking Agriculture and the Environment. Turner BL, Mullaney EJ, editors. CABI; Wallingford: 2007. Phytases: attributes, catalytic mechanisms and applications in: turner; pp. 97–110. [Google Scholar]
  55. Mullaney E.J., Ullah A.H.J. The term phytase comprises several different classes of enzymes. Biochem. Biophys. Res. Commun. 2003;312:179–184. doi: 10.1016/j.bbrc.2003.09.176. [DOI] [PubMed] [Google Scholar]
  56. Nedelciu C.E., Ragnarsdottir K.V., Schlyter P., Stjernquist I. Global phosphorus supply chain dynamics: assessing regional impact to 2050. Glob. Food Sec. 2020;26 doi: 10.1016/j.gfs.2020.100426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Pan Y., Fleet M.E. Compositions of the apatite-group minerals: substitution mechanisms and controlling factors. Rev. Mineral. Geochem. 2002;48:13–49. doi: 10.2138/rmg.2002.48.2. [DOI] [Google Scholar]
  58. Pang F., Li Q., Solanki M.K., Wang Z., Xing Y.X., Dong D.F. Soil phosphorus transformation and plant uptake driven by phosphate-solubilizing microorganisms. Front. Microbiol. 2024;15 doi: 10.3389/fmicb.2024.1383813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. PotashCorp . 2011 Online Overview. PotashCorp; Saskatoon, Can: 2011. Nutrients: phosphate; pp. 39–44.http://www.potashcorp.com/industry_overview/2011 [Google Scholar]
  60. Raghothama K.G. Phosphate acquisition. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999;50:665–693. doi: 10.1146/annurev.arplant.50.1.665. [DOI] [PubMed] [Google Scholar]
  61. Ramos Cabrera E.V., Delgado Espinosa Z.Y., Solis Pino A.F. Use of Phosphorus-Solubilizing Microorganisms As A Biotechnological Alternative: A Review. Microorganisms, 2024;12(8):1591. doi: 10.3390/microorganisms12081591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Rawat P., Das S., Shankhdhar D., Shankhdhar S.C. Phosphate-solubilizing microorganisms: mechanism and their role in phosphate solubilization and uptake. J. Soil. Sci. Plant Nutr. 2021;21(1):49–68. doi: 10.1007/s42729-020-00342-7. [DOI] [Google Scholar]
  63. Raymond N.S., Gómez-Muñoz B., van der Bom F.J., Nybroe O., Jensen L.S., Müller-Stöver D.S., Oberson A., Richardson A.E. Phosphate-solubilising microorganisms for improved crop productivity: a critical assessment. New Phytol. 2021;229(3):1268–1277. doi: 10.1111/nph.16924. [DOI] [PubMed] [Google Scholar]
  64. Reddy P.P. Springer; India: 2014. Mass Production, Formulation Delivery and Commercialization in Plant Growth Promoting Rhizobacteria for Horticultural Crop Protection; pp. 69–83. [DOI] [Google Scholar]
  65. Ribeiro Corrêa T.L., Fernandes de Araújo E. Fungal phytases: from genes to applications. Brazil. J. Microbiol. 2020;51(3):1009–1020. doi: 10.1007/s42770-020-00289-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Richardson A.E., George T.S., Hens M., Simpson R.J. In: Organic Phosphorus in the Environment. Turner BL, Frossard E, Baldwin DS, editors. CABI; Wallingford, UK: 2005. Utilization of soil organic phosphorus by higher plants; pp. 165–184. [Google Scholar]
  67. Richardson A.E., Simpson R.J. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 2011;156:989–996. doi: 10.1104/pp.111.175448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Robinson J.S., Syers J.K., Bolan N.S. Importance of proton supply and calciumsink size in the dissolution of phosphate rock materials of different reactivity in soil. J. Soil Sci. 1992;43:447–459. doi: 10.1111/j.1365-2389.1992.tb00151.x. [DOI] [Google Scholar]
  69. Roser, M., Richie, H., 2023. How has world population growth changed over time? The world population has increased rapidly in recent centuries. But this is slowing. https://ourworldindata.org/population-growth-over-time (Accesed 10.20.23).
  70. Roy T., Rashmi I., Sarkar A. Soil Management For Sustainable Agriculture. Apple Academic Press; 2022. The panorama of phosphorus. Fertilization in crop production; pp. 329–354. [Google Scholar]
  71. Russell D.W. Longman Group Ltd; New York, NY, USA: 1973. Soil Conditions and Plant Growth; p. 849. [Google Scholar]
  72. Saber W.I.K., Ghanem K.M., El-Hersh M.S. Rock phosphate solubilization by two isolates of Aspergillus niger and Penicillium sp. and their promotion to mung bean plants. Res. J. Microbiol. 2009;4(7):235–250. [Google Scholar]
  73. Saeid A., Prochownik E., Dobrowolska-Iwanek J. Phosphorus solubilization by Bacillus species. Molecules. 2018;23(11):2897. doi: 10.3390/molecules23112897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Salgado García S., Núñez Escobar R., Palma López D.J., Debernardi de la Vega H., Mendoza Hernández R.H., Lagunes Espinoza L., del C. Los fertilizantes químicos en Manejo de fertilizantes químicos y orgánicos. Editorial bba (Biblioteca básica de agricultura) Cap. 2012;3:27–52. págs. [Google Scholar]
  75. Sanchez P.A., Uehara G. In: The Role of Phosphorus in Agriculture. Knasawneh FE, Sample EC, Kamrath EJ, editors. American Society of Agronomy; Madison, WI, USA: 1980. Management consideration for acid soils with high phosphorus fixation capacity; pp. 471–514. [Google Scholar]
  76. Sanyal S.K., DeDatta S.K. Chemistry of phosphorus transformations in soil. Adv. Soil Sci. 1991;16:1–120. [Google Scholar]
  77. Schachtman D.P., Reid R.J., Ayling S.M. Phosphorus uptake by plants: from soil to cell. Plant Physiol. 1998;116:447–453. doi: 10.1104/pp.116.2.447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Schneider K.D., van Straaten P., de Orduna R.M., Glasauer S., Trevors J., Fallow D., Smith P.S. Comparing phosphorus mobilization strategies using Aspergillus niger for the mineral dissolution of three phosphate rocks. J. Appl. Microbiol. 2010;108(1):366–374. doi: 10.1111/j.13652672.2009.04489.x. [DOI] [PubMed] [Google Scholar]
  79. Senesi N., Loffredo E. Soil Physical Chemistry. CRC press; 2018. The chemistry of soil organic matter; pp. 239–370. [Google Scholar]
  80. Silva L.I.D., Pereira M.C., Carvalho A.M.X.D., Buttrós V.H., Pasqual M., Dória J. Phosphorus-solubilizing microorganisms: a key to sustainable agriculture. Agriculture. 2023;13(2):462. doi: 10.3390/agriculture13020462. [DOI] [Google Scholar]
  81. Singh B., Boukhris I., Kumar V., Yadav A.N., Farhat-Khemakhem A., Kumar A.…Alghamdi O.A. Contribution of microbial phytases to the improvement of plant growth and nutrition: a review. Pedosphere. 2020;30(3):295–313. doi: 10.1016/S1002-0160(20)60010-8. [DOI] [Google Scholar]
  82. Singh S., Ashoka P., Ahlawat U., Changdeo W.B., Rehsawla R., Naruka A., Sharma D. Mechanisms and Applications of Microbial Biotechnology in Soil Health and Agricultural Productivity: a Review. J. Adv. Biol. Biotechnol. 2024;27(7):1420–1438. doi: 10.9734/jabb/2024/v27i71104. [DOI] [Google Scholar]
  83. Sperber J.I. Solution of mineral phosphate by soil bacteria. Nature. 1957;180:994–995. doi: 10.1038/180994a0. [DOI] [PubMed] [Google Scholar]
  84. Stumm W. Coordinative interactions between soil solids and water - An aquatic chemist's point of view. Geoderma. 1986;38:19–30. doi: 10.1016/00167061(86)90004-2. [DOI] [Google Scholar]
  85. Tian J., Ge F., Zhang D., Deng S., Liu X. Roles of phosphate solubilizing microorganisms from managing soil phosphorus deficiency to mediating biogeochemical P cycle. Biology (Basel) 2021;10(2):158. doi: 10.3390/biology10020158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Timofeeva A., Galyamova M., Sedykh S. Prospects for using phosphate-solubilizing microorganisms as natural fertilizers in agriculture. Plants. 2022;11(16):2119. doi: 10.3390/plants11162119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Timsina J. Can organic sources of nutrients increase crop yields to meet global food demand? Agronomy. 2018;8(10):214. doi: 10.3390/agronomy8100214. [DOI] [Google Scholar]
  88. Tomer S., Suyal D.C., Goel R. In: Plant-Microbe Interaction: An Approach to Sustainable Agriculture. Choudhary D., Varma A., Tuteja N., editors. Springer; Singapore: 2016. Biofertilizers: a timely approach for sustainable agriculture. [DOI] [Google Scholar]
  89. Turan M., Ataoğlu N., Şahιn F. Evaluation of the capacity of phosphate solubilizing bacteria and fungi on different forms of phosphorus in liquid culture. J. Sustain. Agric. 2006;28(3):99–108. doi: 10.1300/J064v28n03_08. [DOI] [Google Scholar]
  90. Turner B.L., Frossard E., Baldwin D.S. CABI Publishing; 2005. Organic Phosphorus in the Environment. Enzymatic Hydrolysis of Organic Phosphorus; pp. 89–112. [Google Scholar]
  91. Van Kauwenbergh J. 2010. Technical Bulletin IFDC-T, 75. [Google Scholar]
  92. Vance C.P. Symbiotic nitrogen fixation and phosphorus acquisition:plant nutrition in a world of declining renewable resources. Plant Physiol. 2001;127:390–397. doi: 10.1104/pp.010331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Vance C.P., Uhde-Stone C., Allan D.L. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. N. Phytol. 2003;157:423–447. doi: 10.1046/j.1469-8137.2003.00695.x. [DOI] [PubMed] [Google Scholar]
  94. Varga T., Hixson K.K., Ahkami A.H., Sher A.W., Barnes M.E., Chu R.K., Battu A.K., Nicora C.D., Winkler T.E., Reno L.R., Fakra S.C., Antipova O., Parkinson D.Y., Hall J.R., Doty S.L. Endophyte-promoted phosphorus solubilization in Populus. Front. Plant Sci. 2020;11 doi: 10.3389/fpls.2020.567918. https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2020.567918 [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Wang Y., Chen Y.F., Wu W.H. Potassium and phosphorus transport and signaling in plants. J. Integr. Plant Biol. 2021 doi: 10.1111/jipb.13053. [DOI] [PubMed] [Google Scholar]
  96. White S., Cordell D.J., Moore D.D. Securing a sustainable phosphorus future for Australia: implications of global phosphorus scarcity and possible solutions. Inst. Sustain. Futures. 2010:1–47. http://hdl.handle.net/10453/35033 Report. [Google Scholar]
  97. White T.J., Dong Z. Structural derivation and crystal chemistry of apatites. Acta Crystallographica Sect. B: Struct. Sci. 2003;59(1):1–16. doi: 10.1107/S0108768102019894. [DOI] [PubMed] [Google Scholar]
  98. Welch S.A., Taunton A.E., Banfield J.F. Effect of microorganisms and microbial metabolites on apatite dissolution. Geomicrobiol. J. 2002;19:343–367. doi: 10.1080/01490450290098414. [DOI] [Google Scholar]
  99. Witzgall K., Vidal A., Schubert D.I., Höschen C., Schweizer S.A., Buegger F., Pouteau V., Chenu C., Mueller C.W. Particulate organic matter as a functional soil component for persistent soil organic carbon. Nat. Commun. 2021;12:4115. doi: 10.1038/s41467-021-24192-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. World Resources Institute., 2008. Eutrophication & hypoxia map data set. Added September 2013. http://www.wri.org/resources/data-sets/eutrophication-hypoxia-map-data-set.
  101. Xu Y., Wu Y., Esquivel-Elizondo S., Dolfing J., Rittmann B.E. Using microbial aggregates to entrap aqueous phosphorus. Trends Biotechnol. 2020;38(11):1292–1303. doi: 10.1016/j.tibtech.2020.03.012. [DOI] [PubMed] [Google Scholar]
  102. Yafetto L. Application of solid-state fermentation by microbial biotechnology for bioprocessing of agro-industrial wastes from 1970 to 2020: a review and bibliometric analysis. Heliyon. 2022 doi: 10.1016/j.heliyon.2022.e09173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Yafetto L., Odamtten G.T., Wiafe-Kwagyan M. Valorization of agro-industrial wastes into animal feed through microbial fermentation: a review of the global and Ghanaian case. Heliyon. 2023 doi: 10.1016/j.heliyon.2023.e14814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Yanes, M.L., Bajsa, N., 2016. Fluorescent Pseudomonas: a natural resource from soil to enhance crop growth and health. Microbial models: from environmental to industrial sustainability, 323–349. 10.1007/978-981-10-2555-6_15. [DOI]
  105. Zaidi A., Ahemad M., Oves M., Ahmad E., Khan M.S. Microbes for Legume Improvement. Springer; Cham, Switzerland: 2010. Role of phosphate-solubilizing bacteria in legume improvement; pp. 273–292. [DOI] [Google Scholar]
  106. Zhang Z., Liao H., Lucas W.J. Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J. Integr. Plant. Biol. 2014;56:192–220. doi: 10.1111/jipb.12163. [DOI] [PubMed] [Google Scholar]
  107. Zhang H., Zhang S.S., Zhang W., Zhu L., Li Y.P., Pan Y. Biomineralization and AHLs-guided quorum sensing enhanced phosphorus recovery in the alternating aerobic/anaerobic biofilm system under metal ion stress. J. Environ. Manage. 2023;325 doi: 10.1016/j.jenvman.2022.116583. [DOI] [PubMed] [Google Scholar]
  108. Zhao Y., Li Y., Yang F. Critical review on soil phosphorus migration and transformation under freezing-thawing cycles and typical regulatory measurements. Sci. Total Environ. 2021 doi: 10.1016/j.scitotenv.2020.141614. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

No data was used for the research described in the article.

Articles from Current Research in Microbial Sciences are provided here courtesy of Elsevier

RESOURCES