Keywords

1 Introduction

Bioavailability of essential nutrients is generally low in cultivated and infertile soils due to resource competition, especially phosphorus (P), which limits the growth of plants (Dubey et al. 2020). Biologically, it is required in plants for their cell division, synthesis of cell organelles, energy and cellular metabolism, synthesis of starch and amino and fatty acids, and N fixation. So, it contributes to root and stalk development, reproduction, fruit/seed quality, disease resistance, and eventually production. Phosphorus is among the less-abundant macronutrients (except N) in the soil (about 0.1% of all elements). It is crucially required by all microorganisms for cell synthesis and metabolism, energy transfer, and signalling (Bünemann et al. 2011).

Contents of bioavailable P in agricultural lands are very little (<0.01–3.07 mg L−1), due to firstly poor P content of parent materials and secondly its high reactivity causing fixation in the mineral matrix (Sharma et al. 2013). This small content fulfils only a little portion of plants’ requirement, so the rest has to be obtained via biotic and abiotic processes for which P-solubilising microflora could be quite helpful. Thus soil microorganisms have developed diverse strategies to enhance P bioavailability. Plants can take up only inorganic P (viz. HPO42−, H2PO4−), while bacteria and fungi also have the capability of consuming low-molecular-weight (LMW) compounds of organic P (Schwöppe et al. 2003). However, protozoa could also take up high-molecular-weight (HMW) compounds of organic P. It infers that a little fraction of organic P pools remains microbially unavailable, so diverse sources of phosphorus in soil could provide ecological niches for various species (Jones and Oburger 2011).

Phosphorus bioavailability in the soil is associated with reversible processes of immobilisation-mineralisation (biological), sorption-desorption (physical), and dissolution-precipitation (chemical). Unfortunately, most of the native P in soil and applied through fertiliser become immobile or fixed via reactions with Al3+ and Fe3+ in low-pH soils and with Ca2+ in alkaline soils (Khan et al. 2015). Therefore, fertiliser’s phosphate use efficiency rarely exceeds 30% with its soluble concentration in the soil around 1.0 mg kg−1 (Mengel et al. 2001) if the total P ranges 500–800 mg kg−1 in soil. Total P content in surface soils (0–15 cm) falls in the range of 50–3000 mg kg−1 contingent upon the type of parent material/soil, land management, and vegetation cover (Sims and Pierzynski 2005). Phosphorus fixation phenomena prevail extensively in the soil as hardly 0.1% of the entire P pool, viz. 0.05% (w/w) is bioavailable, which renders it inaccessible to plants, so its deficiency impedes the growth and yields of plants.

Under this scenario, sustainable crop production and long-term agricultural development demand for exploration of natural processes and biological entities to mobilise the large resource of fixed P accumulated in soil (Dixon et al. 2020). Heterotrophic microbes mainly govern the soil P solubilisation by excreting organic acids and enzymes for P supply to plant roots. Phosphate-solubilising microorganisms (PSM) comprising the P-solubilising bacteria (PSB) as well as P-solubilising fungi (PSF) are used as biofertiliser for P release from immobilised organic and fixed mineral forms in soil (Khan et al. 2014). Sections proceeding below encompass all types of PSM existing in soil, forms of phosphates available for use by PSM, mechanisms of phosphate utilisation, and potentials of native soil P for agricultural production.

2 Phosphate-Solubilising Microorganisms

A larger proportion of total P in the soil is organically bound; therefore, microbes contribute enormously in P turnover. Microorganisms produce carbon dioxide, protons, and secondary metabolites (viz. amino acids, starch, organic acid anions, enzymes, siderophores, phenols, etc.), which catalyse the processes of phosphate solubilisation (Jones and Oburger 2011). Several species of microbes possess great capability of enhancing the organic P cycling through solubilisation of bound organic and mineral P. Research on the PSM spans over a century witnessing the superiority of bacteria (1–50% of total soil bacteria) with greater potential of P solubilisation than fungi (only 0.1–0.5% of total soil fungi) classified as PSM (Chen et al. 2006). Within the total PSM population/species in soil, the PSB outnumber the PSF greatly; however, fungal strains possess higher P-solubilising capability (Gyaneshwar et al. 2002).

More diversified populations of PSM proliferate physically and remain active metabolically in the rhizospheric soils than in other environments. More frequently studied PSM species among bacteria are Bacillus, Burkholderia, Enterobacter, and Pseudomonas, while that of fungi are Aspergillus, Penicillium, and Trichoderma (Bononi et al. 2020). Microorganisms responsible for P acquisition also include ectomycorrhizal and endomycorrhizal fungi. Greater number of metabolically active PSM is found in the rhizosphere than in other ecologies. They exist ubiquitously in forms and population in almost all types of soils depending on the cultural activities, physicochemical properties, organic matter, and phosphate minerals, eventually with their highest populations in cultivated and range lands (Khan et al. 2015).

2.1 Bacteria

Phosphate-solubilising bacteria (PSB) produce organic acids and phosphatases, which mineralise the P-bearing organic materials present in soil (Rodríguez and Fraga 1999). A number of bacteria in fertile soils range from 101 to 1010, and their live biomass could be around 2000 kg ha−1. Structural forms of bacteria found in soil are spherical (cocci, 0.5 μm), rod-shaped (bacilli, 0.5–0.3 μm), or spiral (1–100 μm). Bacilli are the most common type in soil, while spirilla exist scarcely in the natural environments (Baudoin et al. 2002). Relatively more efficient PSB communities in soil are Bacillus, Enterobacter, Pseudomonas, Burkholderia, Azotobacter, and Rhizobium (Jones and Oburger 2011). Strains of Serratia marcescens have been suggested as supersolubiliser for biofertiliser preparation (Ben Farhat et al. 2009).

Multiple P solubilisation mechanisms operating simultaneously have been found in some bacteria as in the case of Gluconacetobacter diazotrophicus (Intorne et al. 2009). Thus, P-solubilising indole acetic acid-producing rhizobacteria (PSIRB) could perform more efficiently than P-solubilising rhizobacteria (PSRB) or indole acetic acid-producing rhizobacteria (IRB) individually (Hariprasad et al. 2009). Similarly, several P-solubilising bacteria proliferating on the outer membrane of mycorrhizal hyphae proliferating in the soil (hyphosphere) add up indirectly to P uptake of mycorrhizae and eventually the plants (Gonzalez-Chavez et al. 2008). Such PSB species may colonise in the mucilage of hyphae, on hyphoplane, among the walls of hyphal layers or within the hyphae (Mansfeld-Giese et al. 2002).

2.2 Fungi

Several non-mycorrhizal fungi isolated from agricultural soils exhibit P-solubilising capability. Among them, inoculation with Aspergillus, Mucor, Penicillium, and Trichoderma species has shown 5–20% improvement in the production of crops (Gunes et al. 2009). Like some ectomycorrhizal fungi, the non-mycorrhizal fungi (e.g. Arthrobotrys, Emericella, Penicillium) could use one or more of these mechanisms for P solubilisation, viz. soil acidification, production of organic acid anions (e.g. citrate, oxalate, gluconate), and release of acid and alkaline phosphatases/phytases (Xiao et al. 2009). Phytase enzyme-producing fungi efficiently hydrolyze the phytases/inositol phosphates, which have the main share in the organic P of soil.

Chaetomium globosum is efficient in the production of phosphatase and phytase for mobilising organic P and has great potential to produce citric, formic, lactic, and malic acid, which are important for about one unit reduction in soil pH (Tarafdar 2019). Aspergillus is known to be the most efficient fungus for producing both types of phosphatases (acid and alkaline). The minimum concentration of fungal released organic acids required to solubilise the phosphates is in the range of 0.2–0.5 mM (Tarafdar 2019). In PSF-treated crops , fungal share in the P uptake is usually greater than that of plants themselves. Extracellular enzymes produced by fungi are more efficient than their intracellular counterparts for P solubilisation.

2.3 Actinomycetes

General characteristics of actinomycetes found in soil include their capability of existing in extreme environmental conditions (e.g. water and salinity stress), production of antibiotics and phytohormones, plant growth promotion, and P solubilisation by some strains (Hamdali et al. 2010). Several species of P-solubilising actinomycetes (PSA) isolated from the rhizosphere soil have been recognised to enhance P use efficiency and stimulate the plant growth when reinoculated. Around 20% genera (including Streptomyces and Micromonospora) among all the actinomycetes are capable of performing P solubilisation process.

Opposite to most fungi, the majority of the PSA does not possess acidifying characteristics. Rather, they release the citrate, formiate, lactate, malate, and succinate anions from respective organic acid and other organic substances associated with P dissolution (Hoberg et al. 2005). They store phosphorus as polyphosphate in their mycelia (Hamdali et al. 2010). Due to their thermotolerance, actinomycetes could be employed preferentially to accelerate the P-release process during compost production (Chang and Yang 2009).

2.4 Mycorrhizae

Mycorrhizal symbiosis among the plant roots and fungal species in soil is usually established in the agricultural and forest ecosystems. The presence of arbuscular mycorrhizal fungi (AMF) is very common in the surface and subsoils, where they establish symbiotic as well as mutualistic associations as found in several plant types (Yang et al. 2018). The rhizosphere is the main habitat for a diversity of beneficial microbes including AMF, which improve P bioavailability and increase the growth of inhabited plants (Zhang et al. 2014). These fungi release protons as well as extend their hyphae for the acquisition of soluble and/or insoluble forms of soil P and then share it with plants especially on P-deficient soils (Smith and Smith 2011). Interaction of such AMF and plant growth-promoting rhizobacteria (PGPR) boosts their activities in the rhizosphere, also to enhance P uptake by the colonised roots of plants (Pierre et al. 2014). By having long aerial mycelia, the AMF transports phosphate from long distances unreachable by plant roots.

The AMF may also release the organic acids and phosphatases that could help solubilise the native P sources unavailable to plants (Tarafdar 2019). Thus, plant root infection with AMF enhances their nutrient absorption efficiency, improves the growth of AMF-infected plants, and influences their root morphology depending upon the mycorrhizal density. The AMF enhance the nodulation in legumes and increase the plant root surface area to approach and uptake more nutrients by the plants. Thus, nitrogen fixation in legumes being dependent on P supply improves with AMF colonisation. The mycorrhizal hyphae also combine the mineral particles of soil and organic materials to make macroaggregates, which join to make more stable macroaggregates (Bibi et al. 2018). The AMF application could reduce the use of P fertiliser.

3 Phosphate Sources vs. Microbial P Solubilisation

Soil microbes have enormous potential for mineralising and solubilising the organic as well as inorganic phosphate compounds, respectively. Various kinds of P minerals as contained in the phosphate rocks exhibit variable solubility. However, the forms of P found in different soils may not be similar to that in phosphate rocks. In the soil’s solid phase, physical and chemical forms of phosphates strongly regulate the efficiency of PSM to mobilise the bound P (Jones and Oburger 2011). As the PSM display differential response to various forms of phosphates, so their inocula are developed according to their ability to dissolve the particular forms of phosphates under field conditions. The following paragraphs comprehend the most dominant P forms in soil:

3.1 Mineralisation of Organic Phosphates

The proportion of organic phosphates in soil varies greatly ranging from 4% (in sandy soils) to 90% (in organic soils) of the total phosphorus contents, but generally it’s 30–65% in mineral soils (Jones and Oburger 2011). Abundant kinds of organic P present in soil are mainly inositol phosphates (dominant, ≥80%), phospholipids (0.5–7.0%), and nucleic acids which account for ≤3% (Quiquampoix and Mousain 2005). Some organic P compounds being less abundant are sugar P, monophosphorylated carboxylic acids, and teichoic acids. Inositol phosphates are component of the insoluble complexes or polymers containing proteins and lipids and have high acidity. Their stability is related to phosphate group counts, which render the higher-order esters being stronger recalcitrant liable to biodegradation and thus higher in abundance. Phospholipids are mostly in the form of phosphoglycerides. Nucleic acids and their derivatives are quickly mineralised, resynthesised, and incorporated into microbial biomass or soil constituents.

Organic soil amendments, viz. municipal biosolids, compost, crop residues, and animal manures, also contribute to P nutrition of plants and soil microorganisms. Nevertheless, P bioavailability from them depends on the P forms present therein and their interaction with soil. Therefore, it has created great interest in the interactive effects of PSM inocula with organic amendments for providing nutrients to the crops. Precise analysis reveals that biosolids contain mainly inorganic P forms, like variscite (Al-P, containing 86% of total P) and less-soluble hydroxylapatite (Ca-P, having 14% of total P), while manures contain 12–68% each of dicalcium phosphate dehydrate and struvite (magnesium ammonium phosphate), 0–18% variscite, and 20–70% organic P as calcium phytate (Ajiboye et al. 2007). Inorganic P component of compost mostly binds to calcium forming the minerals apatite or octacalcium phosphate. Distribution of inorganic P among Al, Fe, and Ca fractions in the compost is also dependent upon the type of additives, e.g. lime, metal salts, etc., which reduce the P solubility and immobilisation (Maguire et al. 2006). Phosphate solubility in organic additives is mostly affected by the equilibrium soil solution and its pH, as at lower pH Fe and Al phosphates render stronger recalcitrant, while Ca phosphate at acidic pH is less recalcitrant. Nonetheless, in addition to phosphate, organic additives supply considerable amounts of carbon and nitrogen, which enhance microbial activities, like respiration, mineralisation, turnover, and biomass build-up (Saha et al. 2008), and accelerate C, N, and P cycling. Increased microbial activity enhances not only the solubilisation of organic and inorganic P found in the organic amendments but also the solubilisation of originally existing P forms in soil too.

Considerable amount in the pool of organic P contributed through the biomass of soil microorganisms. Nevertheless, the contents (mg kg−1) of microbial P present in different soil types range widely from 0.75 (in sandy soils) to 106 (in grasslands) and 169 (in forest litter), which could constitute 0.51–26% of the total P therein (Oberson and Joner 2005). Various phosphate-containing compounds in microbes (as % of the total microbial P) include nucleic acids (30–65%), phospholipids, phosphate esters, and phosphorylated coenzymes (15–20%), along with some P-storage compounds, viz. polyphosphates and teichoic acid found only in Gram-positive bacteria (Bünemann et al. 2011). Phosphorus immobilisation by microorganisms depends more upon C than P limitation; thus P contents in microbial biomass are related to soil C dynamics (Achat et al. 2009). Seasonal variations leading to dry periods, increased soil depth, decreased organic matter, and P fertilisation reduce the biomass P content of microorganisms (Chen et al. 2003).

Nearly 50% among the microbial communities associated with soil and plant root system perform P mineralisation through phosphatase enzymes, e.g. acidic/alkaline phosphatases and phytases (Zineb et al. 2020). Phosphatase enzymes mineralise their substrate of organic phosphate and yield inorganic forms of phosphorus. Major mechanisms for the mineralisation or hydrolysis of organic phosphates and residues to make them bioavailable involve organic anions/acids, siderophores, and phosphatase enzymes produced largely by the microbial population and partially by plant roots (Dodor and Tabatabai 2003). Some microbes, for instance, Enterobacter agglomerans , can perform both functions, viz. hydrolysis of organic P compounds and solubilisation of inorganic P minerals like hydroxyapatite.

3.2 Solubilisation of Phosphate Minerals

Within the growing season, only a small portion (around 1%) from the total soil P assimilates into vegetation biomass, which reflects little P bioavailability to plants (Quiquampoix and Mousain 2005). A fraction of inorganic P ranges 35–70% of the entire soil P being related to the parent material, pH, vegetation, and pedogenesis (Sims and Pierzynski 2005). The pool of organic P rises through soil development processes; however, it declines in greatly weathered and past developed soils. Therefore, soil development processes, P allocation between organic and inorganic P pools, and P forms greatly influence the P accessibility to microbial community and eventually effectiveness of PSM to promote crop growth in the field (Jones and Oburger 2011).

Phosphatic minerals are subjected to solubilisation with several species of saprophytic bacteria and fungi mostly through chelation by both organic and inorganic acids produced by them. Hydroxyl and carboxyl ions from these acids effectively chelate the cations (Al, Fe, Ca) while lower down the pH under basic conditions; resultantly several phosphate compounds are solubilised (Stevenson 2005). Organic acids produced by these microbes are mostly low molecular weight, e.g. gluconic and ketogluconic acids (Deubel and Merbach 2005). The pH mainly in rhizosphere reduces with the release of protons/bicarbonates (anion/cation balance) as well as with the gaseous (O2/CO2) exchange. Thus, organic acids contribute to phosphate solubilisation through pH reduction, cation chelation, and competition with phosphate to find adsorption sites in the soil. Generally, organic acids are more efficient than inorganic acids to solubilise the phosphates if compared to the same level of pH.

3.2.1 Solubilisation of Ca-Bound Phosphates

Sources of primary P minerals in less weathered and unweathered soils having neutral or alkaline pH are calcium phosphates (various types of apatites), e.g. fluorapatite, hydroxyapatite, and francolites (Benmore et al. 1983). Acidification through lowering of soil pH by PSM inocula solubilises Ca phosphates and releases inorganic P. For this purpose, several types of acidifying PSM are employed to enhance the dissolution of phosphate rocks before incorporation into the soil, via inoculation of individual PSM or compost enrichment with microbial consortia (Aria et al. 2010).

Under alkaline conditions, phosphate minerals present in soil as apatites and phosphate from P fertilisers are fixed as phosphates with calcium like Ca3(PO4)2. These compounds and rock phosphates (fluorapatite, francolite) exhibit low solubility rate in soil releasing very little concentration of inorganic P being insufficient to support the normal plant growth. Phosphate solubilisation in alkaline soils undergoes with the joint influence of pH reduction and the release of organic acids (e.g. carboxylic acid). Both these mechanisms operated by soil microorganisms dissociate the bound forms of phosphorus (Stephen and Jisha 2009). Reduced pH or excretion of H+ around microbial cells releases phosphate from P-fixed minerals through proton substitution (with more absorption of cations than anions) or production of Ca2+ (Villegas and Fortin 2002). However, an opposite reaction takes place when anion uptake exceeds that of cations/H+ due to excretion of OH−/HCO3− (Tang and Rengel 2003).

Carboxylic anions released from PSM show greater affinity to Ca, and thus it solubilises more P than the acidification alone. Being an important P solubilisation mechanism, complexing of cations is mainly through pH decrease by organic acids and influenced by nutrition, physiology, growth, and metabolites of the PSM (Reyes et al. 2007). Organic anions and associated protons are important for solubilisation of precipitated P compounds. They would chelate the metal ions attached with complexed P compounds or could release the adsorbed P via ligand exchange reactions. Thus Ca-P releases through joint mechanisms of pH reduction and carboxylic acid production, as the proton release mechanism alone cannot proceed this process (Deubel and Merbach 2005).

3.2.2 Solubilisation of Al and Fe Phosphates

In lower pH and highly weathered soils, the dominant P minerals are Fe and Al phosphates and inorganic P bound and/or occluded by Fe and Al oxy(hydr)oxides (Sims and Pierzynski 2005). Under neutral and acidic soil conditions, Al and Fe oxides/hydroxides greatly influence the P availability, due to rare occurrence of various Fe and Al phosphates, e.g. wavellite, variscite, and strengite. With decreasing pH, positive surface charge of Fe and Al oxides is increased, and strong covalent bonds (chemisorption) are developed through negatively charged P, which renders it recalcitrant to exchange reactions. However, low-molecular-weight (LMW) organic anions (e.g. gluconate and oxalate) excreted from PSM could compete with inorganic P for sorption sites. Further, pH dynamics may influence the surface potential of oxides, resulting in the solubility of inorganic P (Jones and Oburger 2011).

Iron- and aluminium-associated phosphates are solubilised through proton produced by PSM via reducing the negative charge on adsorbing sites that ultimately enhances sorption of negatively charged P ions. Release of protons may also reduce the P sorption due to acidification that increases H2PO4− as compared to HPO42− exhibiting greater affinity to the reactive sites on soil. Carboxylic acids mostly solubilise the Al-P, while Fe-P is solubilised via direct dissolution of phosphate mineral due to anion exchange of PO43− by acid anion, which could chelate both Fe and Al ions attached to phosphate (Henri et al. 2008). Root-associated pseudomonas strains have high-affinity Fe-uptake system depending upon release of Fe3+-chelating agents, viz. siderophores (Khan et al. 2007). Further, carboxylic anions replace the PO43− anions from sorption complexes through ligand exchange, thus chelating both Fe and Al ions attached to phosphate, which after transformation releases bioavailable phosphate for plants. The capability of organic acids for chelating the metal cations is highly affected by these acids’ molecular structure, principally by the abundance of carboxyl and hydroxyl ions.

3.3 Release of Immobilised P from PSM Biomass

It is a general understanding that phosphorus released by PSM is consumed mainly by the plants and soil organisms. Conversely, the fact is that inevitably the greater portion of released P gets assimilated by the PSM biomass itself. Normally, the release of PSM’s immobilised P takes place after their cell death with environmental changes, starvation, or predation by microflora and microfauna. Fluctuation in soil conditions, e.g. drying-rewetting and/or freezing-thawing, results in higher rates of microbial cell lysis (breakdown) causing flush events, which witness a sudden rise of bioavailable P in soil solution (Butterly et al. 2009). Approximately, 30–45% of microbial P (constituting 0.8–1 mg kg−1) is mineralised within a day during the first flush event after drying-rewetting cycles (Grierson et al. 1998). Nevertheless, P bioavailability proceeding the flush events is mainly relying on the P-sorption capability of soil, as the major part of released P could subsequently be immobilised on the solid phase.

Grazing of microorganisms by microbivores (e.g. nematodes, protozoa) also releases microbial P. During a preliminary study, the presence of bacterial grazers caused substantial P mineralisation within a week, while in their absence, vigorous P immobilisation continued beyond 3 weeks without any P release (Cole et al. 1978). Similarly, the presence of organic matter and its C/P ratio render a substantial influence on microbial P immobilisation-mineralisation dynamics (Silvan et al. 2003). Inputs of easily available C sources as fresh organic materials improve the microbial P with subsequent decrease and rise in soil P on the depletion of a substrate (Jones and Oburger 2011). Nevertheless, substrate quality and soil characteristics determine the time passing between P immobilisation and remineralisation, as the dynamics is smaller for stronger recalcitrant organic materials (Oehl et al. 2001).

4 Mechanisms of Phosphate Solubilisation

Phosphate-solubilising efficiency is the ability of PSM to produce organic acids, whose hydroxyl as well as carboxyl ions chelate cations associated with phosphate, so bringing them to soluble state. Phosphate solubilisation in the global P cycling undergoes several mechanisms, which also include organic acids and/or proton release attributed to soil microorganisms. Phosphorus assimilated in the microbial biomass is immobilised for a shorter time, but remineralisation or turnover by microorganisms transforms it in a bioavailable form after some time depending upon the soil conditions. Therefore, P-solubilising microbes are the key players in all the three components of P cycle being operated in soil, viz. mineralisation-immobilisation, dissolution- precipitation, and sorption-desorption. Bioavailability of inorganic P from the P-containing minerals is largely governed by their dissolution properties, which are influenced mainly by the pH and equilibrium reactions in soil solution (viz. sorption and desorption). Whereas, the P bioavailability from organic P materials entirely depends upon the activities of soil microorganisms, e.g. mineralisation, enzymatic hydrolysis, etc. Therefore, various factors and mechanisms are involved in the solubilisation of organic and mineral phosphates in soil as detailed in the following paragraphs:

4.1 Phosphate Release Through pH Dynamics

Microorganisms release protons or hydroxide ions, which change the pH of soil solution as well as mineral nutrient bioavailability. Although phosphate solubilisation via alkalinisation is rarely reported, P solubilisation through microbial acidification rendered by numerous species of bacteria and fungi is well recognised (Ben Farhat et al. 2009) especially if phosphate is associated with calcium. Release of protons sometimes relates to production of organic acid anions, which is enhanced with NH4+ supply (rather than NO3−), and decrease in pH resulting to more P solubilisation (Sharan et al. 2008). Penicillium rugulosum with the assimilation of amino acids as a sole N source also decreased pH in external medium and thus enhanced P mobilisation. Contrastingly in Pseudomonas fluorescens, C source (e.g. glucose vs. fructose) but not N source (e.g. NH4+ vs. NO3−) imparts more impact on proton release (Park et al. 2009).

It reflects that in various microbial species, dissimilar strategies operate in proton release, influenced somewhat by NH4+. Although pH dynamics is a potential P solubilisation mechanism, nevertheless, situations in the field (against in vitro) might not be favourable for enough acidification due to insufficient labile N and C as limiting factors for microbial activity in the bulk soil (Jones and Oburger 2011). Also, especially the calcareous soils have strong pH buffering capacity that might reduce the P solubilisation and reduce the growth of PSM.

4.2 Phosphate Release Via Organic Acid Anions

Just only acidification may not be enough to understand the process of P mineral solubilisation. The LMW organic acid anions (carboxylates) produced from microorganisms are also involved in the solubilisation of inorganic P (Patel et al. 2008). Frequently observed organic acid anions released from PSM are citric, gluconic, glycolic, 2-ketogluconic, lactic, malic, malonic, oxalic, succinic, and tartaric acids (Gyaneshwar et al. 2002). Secretion of protons (rather than organic anions) compensates the loss of negative charge, which reduces the pH of soil. On the other hand, organic anions influence P solubilisation through their negative charges or metal complexation properties. So, inorganic P is mobilised from the metal oxide surface through ligand exchange or solubilisation of iron or aluminium oxides and calcium phosphates, and adsorption/chelation of organic anion liberates the occluded P due to weakening of mineral bonds (Jones and Oburger 2011). Further, adsorption of organic anions on metal oxides reduces positive surface potential that also facilitates the release of adsorbed P.

Organic acids mostly released by bacteria are gluconic and 2-ketogluconic acid, while that by fungi include citric, gluconic, and oxalic acid (Khan et al. 2009). Tricarboxylic acid anions (e.g. citrate) have a greater potential of inorganic P solubilisation due to mineral dissolution mechanism than that of dicarboxylic acids (e.g. gluconate, oxalate), whereas oxalate is more efficient for P mobilisation in calcareous soils due to greater affinity for making Ca precipitates (Ström et al. 2005). Phosphorus mobilisation by organic anions is influenced mainly through soil characteristics (e.g. sorption sites, pH) and properties/quantity of PSM-released organic acid anions, differing greatly from a few micromolars to 100 mM (Gyaneshwar et al. 2002; Patel et al. 2008). The P-solubilising property of organic acid anions mostly declines in soils with higher contents of carbonate and Fe or Al (hydr)oxides (Ström et al. 2005; Oburger et al. 2009).

The LMW carboxylates released from microorganisms as well as roots of a plant are used by microbes as labile C substrate and being removed from the solution; thus their P-mobilisation potential is reduced. For continuous P dissolution during the crop season, organic acid anions must be released by PSM regularly, as their half-life is very short, viz. 0.5–12 h (Jones et al. 2003). Importantly, within high-sorbing soils, breakdown of organic acid anions by microorganisms is greatly reduced (Oburger et al. 2009). In addition to enhancing the growth of microbes and solubilisation of inorganic P, organic acid anions increase the solubility of organic P to make it more prone to enzymatic hydrolysis (Tang et al. 2006).

4.3 Phosphate Release by Enzymes

Phosphorus demand mostly provokes the release of enzymes required for the breakdown of organic P, which is catalysed by phosphatases produced by PSM present in the soil. Usually, extracellular phosphatases instead of intracellular ones release larger amounts of phosphates in soil solution (Nannipieri et al. 2011). Phosphatases or phosphohydrolases represent the large category of enzymes, which catalyse the breakdown of both esters and anhydrides of H3PO4 (Dodor and Tabatabai 2003). Their activities are inhibited at higher contents of orthophosphate (end product), other polyvalent anions (e.g. MoO42−, AsO43−), and some metals, while lower contents of divalent cations (e.g. Ca, Mg, Zn, Co) activate these enzymes (Quiquampoix and Mousain 2005). Moreover, adsorption on soil minerals or organominerals may change enzymes’ conformation and activities. Sorption to solid phase decreases enzymatic activity, but it shields enzymes from microbial decay or thermal inactivation. Clay particles most strongly hold the phosphatases, cluing that soil characteristics (e.g. minerals, SOM, pH) influence PSM-released enzymes, and their activity is not only depending on release rate (Jones and Oburger 2011).

Among the several classes of phosphatase enzymes produced by PSM, phosphatases are the most abundant ones and are categorised as acid and alkaline phosphatases depending upon their pH optima and external conditions (Jorquera et al. 2008). Thus, acid phosphatases are more abundant in low-pH soils, and alkaline phosphatases predominate in neutral- to high-pH soils. The plant roots mostly release acid phosphatases, but rarely alkaline phosphatases, so this could be a niche for PSM. It is very exhaustive to determine the difference among root- and PSM-produced phosphatases; however, microbial phosphatases exhibit higher affinity to organic P compounds as compared to those coming from plant roots (Richardson et al. 2009). Reports on both positive and negative correlations between phosphatase activity and inorganic P concentration in soil highlight the uncertainty and interactive complexity of biochemical processes of P mobilisation (George et al. 2002; Ali et al. 2009).

4.4 Phosphate Release by Siderophores

Siderophores are biochemical complexing agents having a greater affinity for iron, and they are produced by most of soil microbes in response to Fe deficiency. About 500 siderophores have been recognised, and the majority is used by several microbes and plants, while some are utilised by the producing microbes themselves (Crowley 2007). Production of siderophores by PSM is well documented, but not widely known for P solubilisation mechanism (Hamdali et al. 2010). Due to dominance of mineral dissolution against the ligand exchange by organic acid anions as P-solubilising mechanism, siderophores might also be considered for enhancing P bioavailability.

In spite of extensive evidence of Fe mobilisation by siderophores, only one study reported the impact of microbial siderophores on P bioavailability (Jones and Oburger 2011). Improved Fe and P diffusion of two siderophores (desferrioxamine B, desferriferrichrome) and iron-chelating agent EDDHA if compared with water through root simulation method was found long before by Reid et al. (1985). Further, desferriferrichrome enhanced the P diffusion 13-folds against water, while desferrioxamine B rendered very little impact. By keeping in view the large reserves of Fe phosphates in soil, greater P-sorption capacity of Fe (hydr)oxides, and Fe requirements of microbes, the role of siderophore-enhanced P solubilisation is quite obvious.

4.5 Phosphate Release Mediated by Exopolysaccharides

Microbes in soil produce exopolysaccharides (EPS) and biosurfactants mostly to cope with biofilm formation and stress conditions. Recently, nonenzymatic high-molecular-weight (HMW) microbial exudates (viz. mucilage, EPS, etc.) are also being investigated for their effectiveness in P solubilisation from soil components. Gaume et al. (2000) reported that maize root mucilage if adsorbed onto synthetic ferrihydrite reduced the P adsorption continuously, but this mucilage couldn’t mobilise the pre-adsorbed P in a significant amount. Nonetheless, the indirect effect of microbial mucilages has been observed on the P availability via increased soil aggregation and pore connectivity in soil, which facilitates the soil moisture retention and movement (Ionescu and Belkin 2009).

It has been reported that microbially produced EPS can make complexes with the metals in soil variably (Ochoa-Loza et al. 2001), which indicates that they could have some influence on the P solubility in soil. Microbial EPS and organic acid anions produced in pure culture have been found to enhance the dissolution of tricalcium phosphate in a synergistic manner (Yi et al. 2008). The microbial EPS production could be favoured under P-deficient soil conditions, thus being more favoured with N supply rather than available P (Wielbo and Skorupska 2008). Moreover, the rate of phosphate solubilisation depends upon the microbial population/source and EPS contents in soil.

5 Interactive Effects of PSM on Plants

The PSM might also come in competition with growing plants for the uptake of released P from any source. Phosphorus in the soil solution increases under the situation when (a) active P solubilisation from the soil minerals containing large P contents and (b) sum of the SOM mineralisation and remineralisation of organic P detained in microbial biomass exceed P immobilisation (via P uptake and its assimilation in plants/microbial biomass) and sorption onto the surface of soil minerals. These processes involved in P cycling are driven by several physicochemical soil characteristics (e.g. mineral contents, organic matter, texture, structure, temperature, moisture percentage) and vegetation properties, which collectively influence the P bioavailability in soil from PSM inoculation (Jones and Oburger 2011). Since the microbial populations and activities are greater in the rhizosphere, so the combined efforts of microbes and plant roots in proton (or hydroxide) extrusion could enhance the P bioavailability to both. Further, respiration by plant roots and microbes would increase CO2 concentration in the rhizosphere and might cause the pH to decrease.

Tarafdar (2019) mentioned that co-inoculation with compatible fungi could mobilise greater amount of soil P for better plant growth; for instance, the AMF Glomus mosseae combined with Aspergillus fumigatus had a greater activity of phytase enzymes. Plants and PSM have a synergistic association, where microbes provide the soluble P and plant roots supply the carbon compounds (mostly sugars), which are metabolised for microbial proliferation (Pérez et al. 2007). Thus, the presence of PSM in the rhizosphere is highly beneficial for improving crop production. Combined inoculation of Rhizobium and PSM or AMF renders better plant growth than inoculation of each microbe alone in P-deficient soil (Zaidi and Khan, 2006). Positive interactive effects on plant growth through simultaneous application of PSB with AMF or with N-fixing bacteria, e.g. Azospirillum and Azotobacter, have been investigated extensively (Figueiredo et al. 2017; Wahid et al. 2020).

6 Extent of Phosphate Solubilisation in Soil

Contribution of PSM for enhancing the plant growth is influenced mainly by microbial P- mobilisation activities, viz. P uptake followed by its release and P redistribution throughout the soil mass. Numerous studies at the greenhouse and field level have been undertaken to assess the number of phosphates solubilised through inoculation of PSM, and an increase of crop yields up to 70% has been reported (Kumar et al. 2016). The PSB species of P. striata and B. polymyxa mobilised correspondingly 156 and 116 mg P L−1 (Rodríguez and Fraga 1999). Similarly, P. fluorescens released 100 mg P L−1 from Ca3(PO4)2, 92 mg P L−1 from AlPO4, and 51 mg P L−1 from FePO4 (Henri et al. 2008). Acid-producing PSM also improve the solubilisation of phosphatic rocks (Gyaneshwar et al. 2002).

The PSB strains have the capabilities to solubilise the inorganic P from 53 to 42 μg P mL−1 and mineralise organic P ranging 8–18 μg P mL−1 (Tao et al. 2008). Seed inoculation of C. globosum, P. purpurogenum, and E. rugulosa could mobilise 45–60 kg P from soil, rendering 416–25% improvement in the production of various crops (Tarafdar 2019). The PSB applied along with SSP fertiliser and rock phosphate decreased the P fertiliser rate by 25% and 50%, respectively (Sundara et al. 2002). The PSB strains of P. putida, P. fluorescens, and P. fluorescens solubilised 51%, 29%, and 62% phosphate, correspondingly (Ghaderi et al. 2008).

Zineb et al. (2020) reported that Bacillus, Burkholderia, Pseudomonas, and Serratia strains inoculated to rock phosphate solubilised up to 600 mg P mL−1 by producing phytases (16.1–24.8 U mL−1), IAA (up to 39.6 μg mL−1), and siderophores (9–81.1%). The use of PSM inoculum can benefit equivalent to 100–150 kg P ha−1 the fields growing horticultural crops (Gunes et al. 2009). The PSM have a daily potential of mineralising 1–4 mg P kg−1 in the soil; but without any distinction between the enzymatic (biochemical) and biological (microbial turnover) strategies of mineralisation (Oehl et al. 2001).

7 Contribution of PSM in Crop Production

The worldwide consensus is evolving extensively to encourage the adoption of sustainable practices for the management of both agroecosystems and environment. Among them, the high emphasis has been put on the use of beneficial/effective microbes, referred to as biofertilisers or inoculants. These active biological agents containing beneficial microorganisms drive the biogeochemical nutrient cycles. The PSM, mainly the bacteria Bacillus , Pseudomonas, Burkholderia, and Enterobacter and the fungi Trichoderma, Aspergillus, and Penicillium, including ectomycorrhizae and endomycorrhizae have been found beneficial for enhancing the bioavailable P in the cultivated lands as well as improving the production of crops (Bononi et al. 2020). The PSM solubilise the precipitated soil P and fertiliser P contributing significantly to meet P deficiency and enhance crop yields (Sharma et al. 2013).

The combined use of PSB and AMF renders better P uptake both from soil and rock phosphates applied in the field (Cabello et al. 2005). Not only the PSM enhance plant growth by P solubilisation, but they could also increase the N fixation undertaken by crop plants (Ponmurugan and Gopi 2006). The PSB strains of Pseudomonas sp. have been reported to enhance the number and mass of nodules, growth attributes, grain yield, nutrient bioavailability, and their uptake in the soybean crop (Son et al. 2006). In another study, seedling length of Cicer arietinum was increased by PSB application (Sharma et al. 2007). Co-inoculation of PSB and PGPR decreased the P application rate up to 50% in maize (Yazdani et al. 2009). Inoculation with PSB alone raised the biological yield, whereas co-inoculation of the same PSB along with AMF gave the highest yield of barley grains (Mehrvarz et al. 2008). The PSB application improved sugarcane production by 12.6% (Sundara et al. 2002). Inoculation of alpine Carex with Pseudomonas fortinii significantly improved the weight of fresh roots and foliage and P content in shoots (Bartholdy et al. 2001).

Application of PSB in addition to P fertiliser produced 30–40% higher yield of wheat grains than with sole P fertiliser, while inoculation without P fertiliser enhanced 20% yield over control (Afzal and Bano 2008). Pseudomonas putida and AMF co-inoculation in barley also improved the content of leaf chlorophyll (Mehrvarz et al. 2008). With combined inoculation, Bradyrhizobium, G. fasciculatum, and B. subtilis interacted positively for improving plant growth and N and P uptake of green gram, and seed yield was increased by 24% over control (Zaidi and Khan 2006). The PSB strains of Bacillus, Burkholderia, Pseudomonas, and Serratia inoculated to Medicago truncatula increased the dry shoot weight in the range of 40–134% and 13–87% in two soils, and the best results were obtained with their consortium (Zineb et al. 2020).

Currently, Wahid et al. (2020) reported the potential of AMF inoculum containing six species (viz. G. microaggregatum, F. geosporum, C. etunicatum, F. mosseae, R. intraradices, and G. claroideum) and PSB strain Bacillus sp. PIS7 along with phosphate rock on field-grown maize followed by wheat in alkaline soil. Their combined application significantly enhanced the grain yield of crops and P uptake as compared to control and sole applications. In legumes, co-inoculation of Rhizobium and PSM demonstrates great potential in terms of enhancing the nodulation, crop growth and nutrient uptake from chemical fertilisers, e.g. 30% yield improved in soybean (Govindan and Thirumurugan 2005).

Although the strong buffering capacity of soil suppresses the solubilisation of bound P by native microorganisms, efficient PSM inoculants could enhance the microbial activity of P solubilisation contributing significantly in agricultural production. Phosphorus bioavailability in soil depends upon the natural processes of sorption-desorption and immobilization-mineralization. Soil microorganisms contribute enormously in supplying soil phosphorus to the plants through solubilisation of inorganic compounds and mineralization of organic materials. These microorganisms operate two mechanisms in soil, viz., lowering of soil pH via production of organic acids and their anions to solubilise mineral phosphates, and mineralization of organic phosphates via acid phosphatases. Soil enriched with phosphate solubilisers increases the phosphorus bioavailability to the crops. Better efficiency is achieved by co-inoculation of phosphorus solubilising bacteria with other beneficial bacteria, fungi and mycorrhizae. Hence, exploitation of PSM through biofertilisers bears great prospective for utilisation of fixed soil P present hugely in the soil. Similarly, bio-mineralisation of phosphate rocks by the PSM could be an eco-friendly alternative to mineral fertilisers, especially in alkaline soils. So, this chapter concludes that PSM exhibit high potential for the development of a safe biofertiliser product, which could improve the P bioavailability in soil and enhance the plant growth and crop yields to achieve sustainable agricultural production.