REVIEW

published: 02 June 2017

doi: 10.3389/fmicb.2017.00971

Microbial Phosphorus Solubilization

and Its Potential for Use in
Sustainable Agriculture
Elizabeth T. Alori 1 , Bernard R. Glick 2 and Olubukola O. Babalola 3*
1
Department of Biological Sciences, Faculty of Agriculture, Science and Technology, North-West University, Mmabatho,
South Africa, 2 Department of Biology, University of Waterloo, Waterloo, ON, Canada, 3 Food Security and Safety Niche Area,
North-West University, Mmabatho, South Africa

The use of excess conventional Phosphorus (P) fertilizers to improve agricultural

productivity, in order to meet constantly increasing global food demand, potentially
causes surface and ground water pollution, waterway eutrophication, soil fertility
depletion, and accumulation of toxic elements such as high concentration of selenium
(Se), arsenic (As) in the soil. Quite a number of soil microorganisms are capable
of solubilizing/mineralizing insoluble soil phosphate to release soluble P and making
it available to plants. These microorganisms improve the growth and yield of a
wide variety of crops. Thus, inoculating seeds/crops/soil with Phosphate Solubilizing
Microorganisms (PSM) is a promising strategy to improve world food production
Edited by: without causing any environmental hazard. Despite their great significance in soil
Brigitte Mauch-Mani, fertility improvement, phosphorus-solubilizing microorganisms have yet to replace
University of Neuchâtel, Switzerland
conventional chemical fertilizers in commercial agriculture. A better understanding of
Reviewed by:
Oswaldo Valdes-Lopez,
recent developments in PSM functional diversity, colonizing ability, mode of actions and
National Autonomous University judicious application should facilitate their use as reliable components of sustainable
of Mexico, Mexico agricultural systems. In this review, we discussed various soil microorganisms that
Yunuen Tapia Torres,
National Autonomous University have the ability to solubilize phosphorus and hence have the potential to be used
of Mexico, Mexico as bio fertilizers. The mechanisms of inorganic phosphate solubilization by PSM and
*Correspondence: the mechanisms of organic phosphorus mineralization are highlighted together with
Olubukola O. Babalola
olubukola.babalola@nwu.ac.za
some factors that determine the success of this technology. Finally we provide some
indications that the use of PSM will promote sustainable agriculture and conclude that
Specialty section: this technology is ready for commercial exploitation in various regions worldwide.
This article was submitted to
Plant Microbe Interactions, Keywords: mineralization, phosphorus, soil nutrient management, soil microbes, solubilization
a section of the journal
Frontiers in Microbiology
Received: 04 February 2017 INTRODUCTION
Accepted: 15 May 2017
Published: 02 June 2017 Phosphorus (P) is one of the essential elements that are necessary for plant development and
Citation: growth; it makes up about 0.2% of a plant’s dry weight. It is second only to nitrogen among
Alori ET, Glick BR and Babalola OO mineral nutrients most commonly limiting the growth of crops (Azziz et al., 2012; Tak et al.,
(2017) Microbial Phosphorus 2012). On average, the phosphorus content of soil is about 0.05% (w/w); however, only 0.1% of
Solubilization and Its Potential for Use this phosphorus is available for plant use (Zhu et al., 2011). Traditionally, the challenge of soil
in Sustainable Agriculture.
Front. Microbiol. 8:971.
doi: 10.3389/fmicb.2017.00971 Abbreviations: PSM, phosphate solubilizing microorganisms.

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Alori et al. Phosphorus Solubilization for Sustainable Agriculture

phosphorus deficiency is addressed by the application of Ralstonia, Rhizobium (Tajini et al., 2012), Rhodococcus, Serratia,
phosphorus fertilizers. However, the majority of the applied Bradyrhizobium, Salmonella, Sinomonas, and Thiobacillus
fertilizer phosphorus is not available to plants and the addition (Postma et al., 2010; David et al., 2014).
of inorganic fertilizers in excess of the amount that is commonly The microbial fungi that function similarly include
employed to overcome this effect can lead to environmental strains of Achrothcium, Alternaria, Arthrobotrys, Aspergillus,
problems such as, groundwater contamination and waterway Cephalosporium, Cladosporium, Curvularia, Cunninghamella,
eutrophication (Kang et al., 2011). It is therefore of great Chaetomium, Fusarium, Glomus, Helminthosporium,
interest to investigate management strategies that are capable Micromonospora, Mortierella, Myrothecium, Oidiodendron,
of improving phosphorus fertilization efficiency, increase crop Paecilomyces, Penicillium, Phoma, Pichia fermentans,
yields and reduce environmental pollution caused by phosphorus Populospora, Pythium, Rhizoctonia, Rhizopus, Saccharomyces,
loss from the soil. Schizosaccharomyces, Schwanniomyces, Sclerotium, Torula,
Soil microorganisms enhance plant nutrient acquisition. Trichoderma, and Yarrowia (Srinivasan et al., 2012; Sharma et al.,
They are involved in a wide range of biological processes 2013).
including the transformation of insoluble soil nutrients (Babalola Soil fungi have been reported to be able to traverse long
and Glick, 2012a). Some are capable of solubilizing and distances within the soil more easily than bacteria and may be
mineralizing insoluble soil phosphorus for the growth of plants. more important to the solubilization of inorganic phosphate
Apart from chemical fertilization, microbial P-solubilization in soils as they typically produce and secrete more acids,
and mineralization is the only possible way to increase plant- such as gluconic, citric, lactic, 2-ketogluconic, oxalic, tartaric
available phosphorus. In the natural environment numerous and acetic acid, than bacteria (Sharma et al., 2013). In
microorganisms in the soil and rhizosphere are effective at addition, approximately 20% of actinomycetes could solubilize
releasing phosphorus from total soil phosphorus through P, including those in the genera Actinomyces, Micromonospora,
solubilization and mineralization (Bhattacharyya and Jha, and Streptomyces. Algae such as cyanobacteria have also been
2012). This group of microorganisms are referred to as reported to show P solubilization activity (Sharma et al.,
Phosphorus Solubilizing Microorganisms (PSM). Many species 2013).
of soil fungi and bacteria are able to solubilize phosphorus
in vitro and some of them can mobilize phosphorus in
plants (Zhu et al., 2011). PSM increases the bioavailability of BENEFITS OF PHOSPHORUS
soil insoluble phosphorus for plant use (Zhu et al., 2011). SOLUBILIZING MICROORGANISM
They solubilize insoluble inorganic (mineral) phosphorus and
mineralize insoluble organic phosphorus (Sharma et al., 2013). For better utilization of the phosphorus accumulated in soils,
The salt-tolerant or halophilic soil microorganisms that also PSMs that are capable of transforming insoluble phosphorus
exhibit the ability to solubilize insoluble phosphorus facilitate the to soluble forms can function as biofertilizers. This increases
development of saline-alkali soil-based agriculture (Zhu et al., the soluble phosphorus content (Zhu et al., 2012). The use of
2011). phosphorus biofertilizers is a promising approach to improving
The inoculation of soil or crop with phosphate food production through enhancing agricultural yield as it is
solubilizing/mineralizing microorganisms is therefore a better to use an environmentally friendly approach (that is, a
promising strategy for the improvement of plant absorption of paradigm that emphasizes the use of biological soil amendments
phosphorus and thereby reducing the use of chemical fertilizers in place of chemicals) to solve the problems of infertile soil
that have a negative impact on the environment (Alori et al., (Babalola and Glick, 2012a). Figure 1 shows the effect of
2012). inoculation with a PSM (Pseudomonas sp.) on a maize plant. The
growth of maize that was inoculated with PSM was improved
compared to the control that was not inoculated. PSM act as
PHOSPHORUS SOLUBILIZING biofertilizers by making otherwise unavailable P available to
MICROORGANISMS (PSM) growing plants. Phosphorus solubilizing bacteria may also aid
the growth of plants by stimulating the efficiency of biological
A large number of microbial organisms including bacteria, nitrogen fixation, synthesizing phytohormones and enhancing
fungi, actinomycetes, and algae exhibit P solubilization and the availability of some trace elements such as zinc and iron
mineralization ability. Soil bacteria that have been reported (Wani et al., 2007).
to mobilize poorly available phosphorus via solubilization Many PSM inoculation studies have shown both improved
and mineralization include Pseudomonas spp., Agrobacterium plant yield and increased phosphorus uptake both in pot
spp., and Bacillus circulans (Babalola and Glick, 2012b). experiments and under field conditions. In a pot experiment
Other phosphorus solubilizing and mineralizing bacteria where Aspergillus niger was used as a biofertilizer (using wheat
include various strains of Azotobacter (Kumar et al., 2014), husks with 20% perlite as carrier material) the soil colonization
Bacillus (Jahan et al., 2013; David et al., 2014), Burkholderia rate was 5.6 × 106 spores g−1 soil (Wang et al., 2015). The
(Mamta et al., 2010; Zhao et al., 2014; Istina et al., 2015), benefits of adopting microbial management of the rhizosphere
Enterobacter, Erwinia (Chakraborty et al., 2009), Kushneria (Zhu for sustainable agriculture production includes enhancing the
et al., 2011), Paenibacillus (Fernández Bidondo et al., 2011), bioavailability of phosphate to crops, stimulated roots and shoots

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Alori et al. Phosphorus Solubilization for Sustainable Agriculture

FIGURE 1 | Biofertilizer effect of Pseudomonas sp. on maize. (A) Maize not inoculated with a PSM. (B) Maize inoculated with a PSM Pseudomonas sp.

growth, improved root and shoot length, and increased fresh and antifungal compounds (such as PAL, phenolics and flavonoids),
dry shoot weights, P-labeled phosphate uptake, and significant siderophores, antibiotics, hydrogen cyanide and lytic enzymes
improvement of grain and dry matter yields (Rodríguez and all of which enhance inhibition of the growth of plant
Fraga, 1999). Table 1 shows the effect of some PSM on a variety pathogens.
of crops. Phosphate Solubilizing Microorganisms technology improves
Phosphate Solubilizing Microorganisms have considerable the fertility and agricultural use of saline-alkaline soil without
synergistic effect on the growth and development of crops causing any environmental or health hazard that accompanies the
(Tallapragada and Gudimi, 2011). Besides solubilizing P, some continuous use of synthetic fertilizers. Kushneria sp. YCWA18, a
PSM also demonstrate potential as biocontrol agents against strain that is capable of solubilizing both inorganic phosphorus
some plant pathogens. PSM manage the pathogens by producing and organo-phosphorus has also demonstrated moderate

TABLE 1 | Effects of some PSM on crops.

PSM Test crop Result Source

Aspergillus niger Wheat Improved growth Xiao et al., 2013

Serratia sp. Wheat Increased growth Swarnalakshmi et al., 2013
Aspergillus awamoriS29 Mung bean Increased plant growth, total P content, and plant biomass Jain et al., 2012
Burkholderia gladioli Sweetleaf Increased plant growth Mamta et al., 2010
Pseudomonas aeruginosa Chinese cabbage Increased total weight and total length Wang et al., 2010
P. putida Moss Increased growth Tani et al., 2011
Azotobacter chroococcum, Moringaoleifera Increased shoot and root lengths, increased shoot and root Zayed, 2012
Saccharomyces cerevisiae, and dry weights, increased vitamin C and protein content g/g
Bacillus megaterium dry weight leaves
Burkholderia gladioli Oil palm Increased growth and phosphate uptake Istina et al., 2015
Aspergillus niger Penicillium aculeatum Chinese cabbage Increased growth Wang et al., 2015
Bacillus sp. and Pseudomonas sp. Sesame Increased seed yield Jahan et al., 2013
Bacillus thuringiensis Rice Increased shoot length David et al., 2014
Pseudomonas striata and Glomus Soybean-wheat Better root property and increased grain yield Mahanta et al., 2014
fasciculatum
Burkholderia cepacia Maize Improved plant growth Zhao et al., 2014
Azotobacter chroococcum and Wheat Enhanced productivity of wheat Kumar et al., 2014
Bacillus subtilis
P. favisporus TG1R2 Soybeans Increased dry biomass Fernández Bidondo et al., 2011
Rhizobium tropici CIAT899 Beans Enhanced increased; nodule number, nodule mass, shoot Tajini et al., 2012
dry weight, and root growth

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Alori et al. Phosphorus Solubilization for Sustainable Agriculture

halophilic properties and can be used in the development of Other mechanisms of mineral phosphate solubilization by
saline-alkaline based agriculture (Zhu et al., 2011). Aerococcus microorganisms are the production of inorganic acids (such as
sp. strain PSBCRG1-1, Pseudomonas aeruginosa strain PSBI3-1, sulphuric, nitric, and carbonic acids) and the production of
A. terreus strain PSFCRG2-1 and Aspergillus sp. strain PSFNRH-2 chelating substances. It has, however, been reported that the
were all shown to solubilize tricalcium phosphate at different effectiveness of the inorganic acids and the chelating substances
NaCl concentrations (Srinivasan et al., 2012). The PSM in the release of phosphorus in soil is less than that of the
Burkholderia cepacia promoted the growth of maize plants in organic acids. Kim et al. (1997b) therefore reiterate that organic
the presence of NaCl concentrations of up to 5% (Zhao et al., acid production in P solubilization by PSM is not the sole
2014). These organisms all have potential as biofertilizers in reason for the increase in P concentration into culture medium.
saline-alkaline soil based agriculture. In one set of experiments, Furthermore, Mycorrhizal fungi effectively extend plant roots,
for bacterial solubilization, increases in NaCl concentration up aiding crop phosphorus nutrition by increasing the volume of
to 0.8 M resulted in an increase in the percentage of phosphorus soil from which phosphate may be absorbed (Browne et al.,
released but it declined thereafter. On the other hand, with 2009).
increases in NaCl concentration the amount of P released among Another mechanism of microbial phosphate solubilization
phosphate solubilizing fungi was found to decrease throughout reported in the literature is the liberation of enzymes or
the incubation periods (Srinivasan et al., 2012). enzymolysis, the mechanism of P solubilization by PSM in a
medium containing lecithin where the increase in acidity is
caused by enzymes that act on lecithin and produce choline (Zhu
MECHANISMS OF INORGANIC et al., 2011).
PHOSPHATE SOLUBILIZATION BY PSM
A number of theories explain the mechanism of inorganic MECHANISMS OF ORGANIC
phosphate solubilization. As observed in many experiments, the PHOSPHORUS MINERALIZATION
principal mechanism is the production of mineral dissolving
compounds such as organic acids, siderophores, protons, The major source of organic phosphorus in soil is the
hydroxyl ions and CO2 (Rodríguez and Fraga, 1999; Sharma organic matter. The values of organic phosphorus in soil can
et al., 2013). Organic acids produced as described in Figure 2 be as high as 30–50% of the total P and soil organic P
together with their carboxyl and hydroxyl ions chelate cations is largely in the form of inositol phosphate (soil phytate).
or reduce the pH to release P (Seshachala and Tallapragada, Other organic P compounds that have been reported are:
2012); The organic acids are produced in the periplasmic phosphomonoesters, phosphodiesters, phospholipids, nucleic
space by the direct oxidation pathway (Zhao et al., 2014). acids, and phosphotriesters (Rodríguez and Fraga, 1999). In
The excretion of these organic acids is accompanied by a addition, large quantities of xenobiotic phosphonates (pesticides,
drop in pH that results in the acidification of the microbial detergent additives, antibiotics, and flame retardants) that are
cells and the surroundings, hence, P ions are released by regularly released into the environment also contain organic P.
substitution of H+ for Ca2+ (Goldstein, 1994). Surprisingly, Most of these organic compounds are high molecular-weight
Asea et al. (1988) discovered that no correlation exists between materials that are generally resistant to chemical hydrolysis
the pH and the amount of P solubilized. Hence Illmer and and must therefore be bio-converted to either soluble ionic
Schinner (1995) proposed the theory of acidification by H+ . phosphate (Pi, HPO4 2− , H2 PO4 − ), or low molecular-weight
They explained that H+ released is associated with cation organic phosphate, to be assimilated by the cell (Peix et al., 2001).
assimilation. For example, assimilation of NH4 + together with Phosphorus mineralization refers to the solubilization of
H+ excretion brings about P solubilisation (Illmer and Schinner, organic phosphorus and the degradation of the remaining
1995). An alternative mechanism to organic acid production for portion of the molecule. One important theory proposed by
solubilization of mineral phosphates is the release of H+ to the Halvorson et al. (1990) for the solubilisation of organic P is
outer surface in exchange for cation uptake or with the help of the sink theory. This refers to continuous removal of P that
H+ translocation ATPase (Rodríguez and Fraga, 1999). It was result in the dissolution of Ca-P compounds. Consequently,
also reported that the assimilation of NH4+ within microbial the decomposition of P in organic substrates is consistently
cells is accompanied by the release of protons and this results correlated with the P content in the biomass of PSM (Dighton
in the solubilization of phosphorus without the production of and Boddy, 1989). This biological process plays an important
any organic acids (Sharma et al., 2013). Of all the organic acids, role in phosphorus cycling. Different groups of enzymes are
gluconic acid is the most frequent agent of mineral phosphate involved in this. The first groups of enzymes are those that
solubilization; it chelates the cations bound to phosphate, thus dephosphorylate the phosphor-ester or phosphoanhydride bond
making the phosphate available to plants. Gram-negative bacteria of organic compounds. They are non-specific acid phosphatases
solubilize mineral phosphate by direct oxidation of glucose (NSAPs). The most studied among these NSAPs enzymes
to gluconic acid (Goldstein, 2000). Pyrroloquinoline quinone released by PSM, are the phosphomonoesterases also referred
(PQQ) acts as a redox cofactor in glucose dehydrogenases to as phosphatases (Nannipieri et al., 2011). These enzymes can
(GDH) resulting in phosphate solubilisation (Rodríguez et al., either be acid or alkaline phosphomonoesterases (Jorquera et al.,
2000). 2011). The pH of most soils where phosphate activities were

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Alori et al. Phosphorus Solubilization for Sustainable Agriculture

FIGURE 2 | Schematic representation of the organic acids that may be produced by PSM and used to solubilize inorganic forms of phosphate.

reported ranges from acidic to neutral values. This signifies that solubiliztion while 28◦ C was reported by Kang et al. (2002),
acid phosphatases play the major role in this process (Rodríguez and Varsha (2002). In addition, others including Kim et al.
and Fraga, 1999). (1997a), Rosado et al. (1998), Johri et al. (1999), and Fasim
Another enzyme produced by PSM in the process of organic et al. (2002), have recorded 30◦ C as the best temperature for P
P mineralization is phytase. This enzyme is responsible for solubilization. Nahas (1996) and Nautiyal et al. (2000) reported P
the release of phosphorus from organic materials in soil (plant solubilization at extreme temperature of 45◦ C in desert soil while
seeds and pollen) that are stored in the form of phytate. Johri et al. (1999) reported solubilization at a low temperature of
Phytate degradation by phytase releases phosphorus in a form 10◦ C.
that is available for plant use. Plants generally cannot acquire Among other factors influencing microbial phosphate
phosphorus directly from phytate, however, the presence of PSM solubilization are interactions with other microorganisms in the
within the rhizosphere may compensate for a plant’s inability to soil, the extent of vegetation, ecological conditions, climatic zone
otherwise acquire phosphorus directly from phytate (Richardson soil types, plant types, agronomic practices, land use systems,
and Simpson, 2011). and the soil’s physicochemical properties such as organic matter
and soil pH (Seshachala and Tallapragada, 2012). Phosphorus
is solubilized faster in warm humid climates and slower in cool
FACTORS INFLUENCING MICROBIAL dry climates. A well-aerated soil will more readily permit rapid
PHOSPHATE SOLUBILIZATION phosphorus solubilisation compared to a saturated wet soil. The
land use system is the use that the farmland has been previously
The ability of PSM to transform insoluble organic and inorganic committed to, such as cropping or livestock activities or even
phosphorus is associated with, the nutritional richness of the mixed use. Recently, Zhang et al. (2014) reported that adding
soil, and the physiological and growth status of the organism. small amounts of inorganic phosphorus to the rhizosphere could
PSM from soils from environmental extremes such as saline- drive phytic acid mineralization by bacteria and thereby improve
alkaline soils, soil with a high level of nutrient deficiency, or plant phosphorus nutrition. Lime and compost, used as a soil
soil from extreme temperature environments have the tendency improver, also had positive effects on phosphate solubilizers.
to solubilize more phosphate than PSM from soils from more Phosphorus Solubilizing Bacteria population richness and
moderate conditions (Zhu et al., 2011). There has been a diversity, according to Azziz et al. (2012), were more abundant
conflicting report on the influence of temperature on phosphorus and diverse following crop rotation. Soil rich in organic matter
solubilization by microbes. White et al. (1997) found 20–25◦ C as will favor microbial growth and therefore favors microbial
the optimum temperature for maximum microbial phosphorus phosphorus solubilisation. Soil pH values between 6 and 7.5 are

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Alori et al. Phosphorus Solubilization for Sustainable Agriculture

best for P-availability, this is because at pH values below 5.5 and CONCLUSION
between 7.5 and 8.5 limits P from becoming fixed by aluminum,
iron, or calcium, and hence, not being available for plant use. This review has shown that phosphate-solubilizing
A negative correlation was observed between the amount of microorganisms have tremendous potential as Bio-fertilizers.
phosphate solubilized by B. cepacia SCAUK0330 and the pH drop Mobilizing soil inorganic phosphate and increasing its
that is associated with this process. The pH drop leads to an bioavailability for plant use by harnessing soil PSM promotes
increase in phosphate solubilization. At pH 3.12, 452 µg·mL−1 sustainable agriculture, improves the fertility of the soil, and
of phosphorus was solubilized, and when 154 µg·mL−1 of P was hence increases crop productivity. The use of PSM as microbial
solubilized the pH value was 4.95 (Zhao et al., 2014). Research inoculants is a new horizon for better plant productivity. PSM
has also shown that microbial phosphate solubilization largely technology can contribute to low-input farming systems and a
depends on the kinds of metabolite produced and its rate of cleaner environment. However, there is need to develop PSB
release (Zhu et al., 2011). technologies specific to various regions and this should be
communicated to farmers in a relatively short time.

FUTURE PROSPECTS
AUTHOR CONTRIBUTIONS
As additional insights are gained regarding PSM and the
mechanisms that they use, there is every reason to believe that All authors listed, have made substantial, direct and intellectual
the use of PSM as biofertilizers will likely improve their use, contribution to the work, and approved it for publication.
as effective and important components in the establishment of
sustainable soil management systems. The focus of consumers
of agricultural produce is on the health, quality and nutritional ACKNOWLEDGMENTS
value of those products. Thus, the employment of PSM as
biofertilizers is an option that can increase food production North-West University granted ETA post-doctoral support. BG
without imposing any health hazard, and at the same time and OB would like to thank the Natural Sciences and Engineering
conserve the environment. It is essential that researchers Research Council of Canada and National Research Foundation,
continue to learn more about PSM and, immediately, translate South Africa for grant (UID81192), respectively, for funds that
this knowledge into a form that can readily be used by farmers. have supported research in their labs.

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phosphate-solubilizing Pichia farinose FL7. Bioresour. Technol. 11, 410–416. Copyright © 2017 Alori, Glick and Babalola. This is an open-access article distributed
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