Journal of Soil Science and Plant Nutrition

https://doi.org/10.1007/s42729-020-00342-7

REVIEW

Phosphate-Solubilizing Microorganisms: Mechanism and Their Role

in Phosphate Solubilization and Uptake
Pratibha Rawat 1 & Sudeshna Das 1 & Deepti Shankhdhar 1 & S. C. Shankhdhar 1

Received: 25 February 2020 / Accepted: 9 September 2020

# Sociedad Chilena de la Ciencia del Suelo 2020

Abstract
Phosphorus is the second most critical macronutrient after nitrogen required for metabolism, growth, and development of plants.
Despite the abundance of phosphorus in both organic and inorganic forms in the soil, it is mostly unavailable for plant uptake due
to its complexation with metal ions in the soil. The use of agrochemicals to satisfy the demand for phosphorus to improve crop
yield has led to the deterioration of the ecosystem and soil health, as well as an imbalance in the soil microbiota. Consequently,
there is a demand for an alternate cost-effective and eco-friendly strategy for the biofortification of phosphorus. One such strategy
is the application of phosphate-solubilizing microorganisms which can solubilize insoluble phosphates in soil by different
mechanisms like secretion of organic acids, enzyme production, and excretion of siderophores that can chelate the metal ions
and form complexes, making phosphates available for plant uptake. These microbes not only solubilize phosphates but also
promote plant growth and crop yield by producing plant-growth-promoting hormones like auxins, gibberellins, and cytokinins,
antibiosis against pathogens, 1-aminocyclopropane-1-carboxylic acid deaminase which enhances plant growth under stress
conditions, improving plant resistance to heavy metal toxicity, and so on. Pyrroloquinoline quinine (pqq) and glucose dehydro-
genase (gcd) are the representative genes for phosphorus solubilization in microorganisms. The content presented in this review
paper focuses on different mechanisms and modes of action of phosphate-solubilizing microorganisms, their contribution to
phosphorus solubilization, growth-promoting attributes in plants, and the molecular aspects of phosphorus solubilization.

Keywords Phosphate-solubilizing microorganisms . Organic acids . 1-Aminocyclopropane-1-carboxylic acid deaminase .

Phosphorus solubilization . Phosphatases

1 Introduction adsorption, and interconversion to organic form (Kishore

Phosphorus is an indispensable macronutrient necessary for
key metabolic processes in plants, such as cell division, ener-
gy generation, biosynthesis of macromolecules, membrane
integrity, signal transduction, and photosynthesis. It also plays
a role in respiration in plants (Khan et al. 2010) and fixation of
nitrogen in leguminous crops (Hutchins et al. 2019).
Phosphorus in top soil generally accounts for 50 to
3000 mg kg− 1 of soil, yet only 0.1% of total phosphorus is
available for plant uptake (Zou et al. 1992; Zhu et al. 2018),
due to precipitation with cations in soil, immobilization,
* S. C. Shankhdhar
shankhdhar.sc@rediffmail.com
1
Department of Plant Physiology, College of Basic Sciences &
Humanities, G. B. Pant University of Agriculture & Technology,
Pantnagar, Uttarakhand, India
et al. 2015). Consequently, there has been an increase over
the years in the demand for and use of phosphatic fertilizers to
maintain a continuous supply of phosphorus in plants, as il-
lustrated in Table 1. However, a huge proportion of phosphat-
ic fertilizers precipitate in the soil. These contain a variety of
heavy metals (Azzi et al. 2017), so that heavy metals accumu-
late in the soil, causing a detrimental effect on soil fertility and
animal and consumer health, as well as eutrophication and a
widening carbon footprint (Huang et al. 2017a). In the circum-
stances, there is an exigency for an eco-friendly approach that
can achieve the same goal as synthetic fertilizers, without the
cons. Phosphate-solubilizing microorganisms (PSMs) are bio-
inoculants that are promising substitutes for agrochemicals,
which adopt different strategies to solubilize insoluble phos-
phorus to soluble form and can reduce the phosphate fertilizer
input in agricultural land, as evident in the findings of Hussain
et al. (2019). The researchers observed that interaction of
PSMs (Pseudomonas, Mycobacterium, Bacillus, Pantoea,
 J Soil Sci Plant Nutr

Table 1 World phosphate

fertilizer demand (thousand 2016 2017 2018 2019 2020 2021 2022
tonnes P2O5) forecast (FAO
2019) World 44481 45152 45902 46587 47402 48264 49096
Africa 1676 1827 1942 2030 214 2194 2274
Americas 12121 12237 12488 12713 12932 13165 13387
North America 5007 5023 5135 5183 5220 5261 5294
Latin America & Caribbean 7114 7213 7353 7530 7712 7904 8094
Asia 25445 25719 26100 26357 26774 27217 27662
West Asia 1148 1104 1091 1072 1065 1059 1054
South Asia 8586 8801 9118 9323 9690 10071 10457
East Asia 15711 15814 15891 15962 16019 16087 16151
Europe 4030 4048 4089 4180 4262 4355 4435
Central Europe 793 817 827 843 868 908 940
West Europe 1820 1784 1771 1774 1772 1769 1766
East Europe 1418 1447 1490 1563 1622 1677 1729
Oceania 1208 1322 1283 1307 1321 1333 1337

P2O5 phosphorus pentoxide

Rhizobia, and Burkholderia) and phosphate fertilizer im-
proved the wheat grain yield (22%) and phosphorus uptake
(26%), while reducing the fertilizer input by 30% (from 120 to
90 kg P2O5 ha− 1). Moreover, these biofertilizers are safe and
non-toxic to the environment. PSMs secrete organic acids like
citric acid, oxalic acid, and succinic acids; enzymes like phos-
phatases and phytases; and ion chelators like siderophores that
readily make phosphorus available to plants (Tomer et al.
2016). Plant growth promotion is another attribute of PSMs.
They enhance the overall growth and development of plants in
both stressed and non-stressed environments. Many studies
have reported that PSMs could solubilize potassium, enhance
nitrogen fixation, and produce plant growth regulators like
auxins, cytokinins, and gibberellins while also protecting
plants from pathogens, as they excrete antibiotics and antifun-
gals, and they are exceptional biocontrol agents. Moreover,
they can also aid in the bioremediation of heavy metal con-
taminated soil. Many PSMs secrete 1-aminocyclopropane-1-
carboxylic acid (ACC) deaminase enzyme that reduces the
stress ethylene symptoms in plants during stress conditions.
Such tiny organisms can therefore perpetuate ecological bal-
ance, produce safe food, and satisfy the demands of a sustain-
able agriculture plan (Rawat et al. 2020). This review paper
highlights the diverse means PSMs use for phosphorus disso-
lution, as well as their plant growth encouraging traits.
2 Phosphorus Pool in Soil
Phosphorus occurs in soil in both organic and inorganic forms
through various soil processes, as depicted in Fig. 1. Organic
phosphorus constitutes more than 20% of total phosphorus in
the soil, being derived from biological metabolic processes
like orthophosphate assimilation and microbial, plant, or ani-
mal residues. These are categorized on the phosphorus bond
basis into three classes: (a) phosphate esters (sugar phos-
phates, phospholipids, nucleic acids, inositol phosphates);
(b) phosphonatases (C–P bonds); and (c) phosphoric acid an-
hydrides (adenosine triphosphates and adenosine diphos-
phates) (Huang et al. 2017b). Inorganic phosphorus in the soil
comprises phosphates bound to minerals like calcium phos-
phate, aluminum phosphate, and iron phosphate, which are the
predominant source of phosphorus for young plants (Boitt
et al. 2018).
Technological advancement in agricultural practices and
population pressure have introduced abrupt changes into the
phosphorus dynamics in soil. Around 67% of the world’s
agricultural land is deficient in phosphorus (Dhillon et al.
2017). Application of agrochemicals in soil is hazardous,
whereas phosphorus recovery efficiency of the crops is only
10–20% (Rose et al. 2010). Generally, the maximum phos-
phorus concentration (0.1–5 mg P l− 1) is attained near the soil
surface due to the input of fertilizer. Conversely, subsoils are
deficient in dissolved phosphorus (< 0.1 mg P l− 1) (Bol et al.
2016). High fixation capacity of soil and inactivation of the
applied phosphorus in soil due to immobilization, precipita-
tion, and complexation results in scarcity of available phos-
phorus to plants. Aluminum and iron phosphates are the lead-
ing forms of phosphorus in acidic soil, whereas calcium phos-
phates are present in alkaline soil (Kumar and Shastri 2017).
Soil pH is a pivotal factor in ascertaining the immobilization
of phosphorus in soil (Zhu et al. 2018). Moreover, labile or-
ganic carbon, which acts as a source of energy for microor-
ganisms, is also one of the prominent factors that magnify the
phosphorus mobilization in paddy soil through microbial iron
(III) reduction (Khan et al. 2019a). For healthy crop growth
J Soil Sci Plant Nutr
Fig. 1 Different forms of phosphorus and its dynamics in soil. P phosphorus, Pi inorganic phosphorus, Po organic phosphorus, Fe iron, Fe-P iron-
phosphate, Al-P aluminum phosphate, Ca-P calcium phosphate
and yield, a critical (optimum) phosphorus concentration in
soil should be maintained, as presented in Table 2. Owing to
the current scenario of phosphorus in the soil, there is a need
for an alternative strategy for phosphorus availability instead
of chemicals which are unable to satisfy crop phosphorus
demand and that destroy soil and microbiome properties.
3 Phosphate-Solubilizing Microorganisms
(PSMs)
Soil is a hotspot of the diversified microbiome. PSMs are the
organisms that have the potential to convert insoluble phos-
phorus into a plant-available form. These are copious in soil,
and their potential for P solubilization can be analyzed
through qualitative and quantitative methods (Mehta and
Nautiyal 2001). PSMs are diversified in nature, as listed in
Table 3. Bacteria belonging to the genera Pseudomonas,
Enterobacter, and Bacillus (Biswas et al. 2018; Buch et al.
2008), Serratia and Pantoea (Sulbaran et al. 2009),
Rhizobium, Arthrobacter, and Burkholderia, and Rahnella
aquatilis HX2 (Liu et al. 2019a; Zhang et al. 2019),
Table 2 Critical (optimum) value
of phosphorus for different Cropping system
cropping system
Bean-based cropping system
Rapeseed-based cropping system
Maize-based cropping system
Wheat-based cropping system
Pea-based cropping system
Rice-based cropping system
Cotton-based cropping system
Leclercia adecarboxylata (Teng et al. 2019a), and fungi like
Penicillium brevicompactum and Aspergillus niger (Rojas
et al. 2018; Whitelaw 1999), and Acremonium, Hymenella,
and Neosartorya (Ichriani et al. 2018) are potent PSMs.
These soil microbes perform a significant role in soil by their
metabolic activities and are a remarkable part of integrated
nutrient management in the soil, as they improve the plant’s
nutrient acquisition from the soil. These microorganisms serve
as potent biofertilizers that improve the agricultural yield in
harmony with ecological concerns (Rajwar et al. 2018). PSMs
are diverse in their functions. They are also known for plant
growth promotion through the production of growth-
promoting compounds. Various experiments have been con-
ducted to analyze the plant growth promotion effects of PSMs,
both under stressed and normal conditions, as listed in
Table 4.
PSMs produce growth-promoting hormones like auxins,
cytokinins, and gibberellins which promote cell division, cell
differentiation, shoot growth, root development, flowering,
germination, and xylem differentiation (Puri et al. 2020). A
novel strain like Bacillus tequilensis has been reported to se-
crete plant growth hormones like abscisic acid, auxin, and
Critical phosphorous limit (kg P ha− 1) References
21.2 Athokpam et al. (2018)
31.0–38.0 Swami and Maurya (2018)
17.0 Chandrakala et al. (2017)
39.4–57.1 Singh et al. (2016)
14.30–45.0 Athokpam et al. (2016)
19.2–24.8 Biswas et al. (2017)
11.9 Rochester (2010)
 J Soil Sci Plant Nutr

Table 3 Diversity of phosphate-solubilizing microorganisms in the soil

Bacteria References

Klebsiella variicola, Ochrobactrum pseudogrignonense Nacoon et al. (2020)

Staphylococcus haemolyticus, Staphylococcus cohnii Hii et al. (2020)
Pseudomonas putida, Leclercia adecarboxylata Teng et al. (2019b)
Rahnella aquatilis HX2, Burkholderia cenocepacia Liu et al. (2019a); Zhang et al. (2019)
Pseudomonas fulva, Enterobacter sp. Munir et al. (2019); Suleman et al. (2018)
Bacillus megaterium, Bacillus licheniformis, Rhizobium sp. Biswas et al. (2018); Li et al. (2018)
Arthrobacter defluvii, Pseudomonas frederiksbergensis, Rhodanobacter sp., Bacillus cepacia, Vibrio Zheng et al. (2019)
paradoxus
Acinetobacter rizosphaerae, Tetrathiobacter sp. Gulati et al. (2010); Kumar et al. (2013)
Pantoea sp., Enterobacter sp. Park et al. (2011)
Pseudomonas chlororaphis, Rhodococcus sp., Cupriavidus, Arthrobacter sp., Acinetobacter sp., Bacillus Yu et al. (2011)
cereus
Pseudomonas fragi, Pseudomonas trivalis, Pseudomonas lurida, Pseudomonas sp., Exiguobacterium Selvakumar et al. (2009)
acetylicum
Pseudomonas poae, Pseudomonas fluorescens, Pseudomonas trivalis, Pseudomonas sp. Gulati et al. (2008)
Micrococcus, Bacillus sp. Chatli et al. (2008)
Xanthomonas campestris Sharan et al. (2008)
Arthrobacter sp., Rhodococcus erythropolis, Bacillus megaterium, Serratia marcescens, Chen et al. (2006)
Chryseobacterium sp.
Enterobacter aerogenes, Pantoea agglomerans, Klebsiella sp. Chung et al. (2005)
Pseudomonas corrugata, Mycobacterium phlei Egamberdiyeva and Hoflich (2003);
Pandey and Palni (1998)
Bacillus atrophaeus, Bacillus amyloliquefaciens, Vibrio proteolyticus, Paenibacillus macerans, Vazquez et al. (2000)
Pseudomonas stutzeri, Enterobacter taylorae, Kluyvera cryocrescens, Enterobacter aerogenes,
Chryseomonas luteola, Xanthobacter agilis, Enterobacter asburiae
Fungi
Penicillum sp. PK112, Trichoderma harzianum OMG08 Mercl et al. (2020)
Aspergillus aculeatus P93, Penicillium daleae, Aspergillus versicolor Adhikari and Pandey (2019)
Acremonium, Hymenella, Neosartorya Ichriani et al. (2018)
Penicillium brevicompactum, Aspergillus niger Rojas et al. (2018)
Penicillium oxalicum Li et al. (2016)
Aspergillus candidus, Aspergillus nidulans, Aspergillus wentii, Aspergillus sydowii Rinu and Pandey (2010)
Penicillium expansum, Mucor ramosissimus, Candida krissii Xiao et al. (2009)
Aspergillus fumigatus, Aspergillus niger, Penicillium sp. Chatli et al. (2008)
Glomus clarum, Glomus geosporum Souchie et al. (2006)
Trichoderma virens, Trichoderma viride Rudresh et al. (2005)
Penicillium radicum, Penicillium bilaiae Wakelin et al. (2004)
Mortierella sp., Glomus aggregatum Osorio and Habte (2001)
Penicillium pinophilum, Aspergillus sp. Wahid and Mehana (2000)
Vesicular arbuscular mycorrhizae
Rhizophagus irregularis MUCL 43194 Zhang et al. (2019)
Glomus fasciculatum, Entrophospora colombiana Sharma et al. (2013)
Actinomycetes
Streptomyces thermos-carboxydus, Streptomyces werraensis, Streptomyces ambifaria Hamim et al. (2019)
Streptomyces fulvissimus, Streptomyces, Streptoverticillium Nandimath et al. (2017)
Microbacterium lacusdiani sp. Zhang et al. (2017)
Cyanobacteria
Anabaena variabilis, Westiellopsis prolifica Yandigeri et al. (2010)
Calothrix braunii, Nostoc sp., Scytonema sp. Sharma et al. (2013)
J Soil Sci Plant Nutr

Table 4 List of phosphate-solubilizing microorganisms, their host, phosphate-solubilizing ability and growth-promoting attributes

Phosphate-solubilizing Host plant Amount of Plant growth promotion References

microorganisms phosphorus
solubilized
(μg ml− 1)

Serratia plymuthica Vicia faba L. 450.00 Improved phosphorus uptake in roots and shoots, Borgi et al. (2020)
BMA1 plant biomass and plant height increment,
enhanced carotenoid and chlorophyll content in
leaves
Streptomyces laurentii Sorghum bicolour L. 206.65 Siderophore production, IAA production, ACC Kour et al. (2020)
deaminase activity, potassium solubilization,
osmolyte formation like glycine betaine, total
soluble sugar production under drought stress
Pantoea agglomerans Capsicum annuum 851.61 IAA production, phytase production, increment in Li et al. (2020)
root shoot biomass, leaf area and leaf number
Pseuomonas sp. P34 Triticum aestivum 101.60 Siderophore production, enhancement in root traits Liu et al. (2019b)
and dry matter accumulation of plant
Klebsiella sp. MR13 Oryza sativa L. 392.00 Increase in dry matter production, grain yield of crop Rasul et al. (2019)
Bacillus megaterium Brassica napus 119.37 Increment in phosphorus content and biomass Zheng et al. (2019)
CS22 production
Bacillus sp. STJP Mentha arvensis L. 610.33 Siderophores, IAA, HCN production, increment in Prakash and Arora
dry matter and yield (2019)
Bacillus licheniformis Vigna radiata 222.00 Enhancement in seed germination IAA and ammonia Biswas et al. (2018)
(MF 589720) production, improves resistance of host plant to
copper and zinc toxicity
Azospirillum brasilense Triticum aestivum 18.00 IAA, peroxidase, ascorbate peroxidase production Kadmiri et al. (2018)
DSM1690 under salt stress condition
Serratia nematodiphila Vigna mungo, Pisum 86.00 ACC deaminase, siderophores, IAA production, Saikia et al. (2018)
RJ10 sativum increase in biomass of crop under drought stress
condition
Bacillus sp. CP h60 Cicer arietinum 753.00 ACC deaminase, IAA, increase in number and dry Ditta et al. (2018)
weight of nodules, root shoot biomass increment
Pseudomonas fluorescens Triticum aestivum 29.80 IAA, peroxidase, ascorbate peroxidase production Kadmiri et al. (2018)
MS-01 under salt stress condition
Paenibacillus Triticum aestivum 490.00 IAA production, increase in plant root and shoot Kudoyarova et al.
illinoisensis IB 1087 biomass (2017)
Serratia sp. 5D Cicer arietinum 119.94 IAA production, improvement in grain yield, straw Zaheer et al. (2016)
yield and nodule dry weight
Pantoea sp. Solanum lycopersicum 956.00 Enhancement in root and shoot biomass, total dry Sharon et al. (2016)
matter yield
Aspergillus niger S-36 Cicer arietinum 366.25 Augmentation of root shoot biomass, chlorophyll Saxena et al. (2015)
Bacillus sp. RM-2 345.77 content of inoculated plants
Pseudomonas putida Pisum sativum 319.00 Shoot biomass increment, high seed protein content Ahmad et al. (2013)
PSE3 and high phosphorus in shoots
Pseudomonas strain Lentil (cv. VL Masoor 38.33 IAA and siderophore production, increment in root Selvakumar et al.
RT5RP2 507) 35.40 shoot biomass, yield and nutrient uptake (2013)
Pseudomonas strain augmentation in treated plants
RT6RP
Bacillus KAP5 Triticum aestivum 753.00 Increment in root traits, root length, root biomass, Baig et al. (2012)
Bacillus KAP6 698.00 yield enhancement (38.5%), improved
phosphorus uptake in shoot, root, and grains of
inoculated plants
Penicillium oxalicum Triticum aestivum, Zea 586.00 Shoot height of inoculated wheat plants enhanced 1.5 Singh and Reddy (2011)
mays L. times compared to control, yield increment of 42%
in wheat compared to control. In maize, increment
in root shoot biomass, 82 percent yield increment
compared to control
Staphylococcus scirui, Oryza sativa L. 192.00 Yield increment in treated plants followed by Rajapaksha and
Bacillus pumilus, enhanced phosphorus uptake in shoot, root, grains Senanayake (2011)
Bacillus subtilus,
Bacillus cereus
Pseudomonas lurida Triticum aestivum 340.00 Siderophores and IAA production, improved nutrient Selvakumar et al.
M2RH3 uptake and root shoot biomass of treated seedlings (2011)
 J Soil Sci Plant Nutr

Table 4 (continued)

Phosphate-solubilizing Host plant Amount of Plant growth promotion References

microorganisms phosphorus
solubilized
(μg ml− 1)

Enterobacter aerogenes Vigna unguiculata L. 76.30 IAA, siderophores, HCN production, seedlings’ root Deepa et al. (2010)
sp. NII-0907 60.10 shoot length and biomass , leaves’ diameter
Enterbacter aerogenes 79.50 improved in inoculated plants
sp. NII-0929
Enterobacter asburiae sp.
NII-0934
Acinetobacter Zea mays L. 750.00 Plant height and root shoot length increment, higher Gulati et al. (2010)
rhizosphaerae BIHB root shoot phosphorus content in treated plants.
723 Available calcium and phosphorus content of soil
was higher in inoculated treatment
Azotobacter sp. PSRB7 Lycopersicum 143.00 High root shoot biomass and phosphorus uptake in Hariprasad and
Enterobacter sp. PSRB19 esculentum 141.00 inoculated plants, reduced incidence of Fusarium Niranjana (2009)
Pseudomona putida 100.00 wilt in treated seedlings compared to control
PSRB6 126.00
Bacillus subtilis PSRB32

IAA indole acetic acid, ACC 1-aminocyclopropane-1-carboxylic acid, HCN hydrogen cyanide

gibberellins (GA1, GA3, GA5, GA18, and GA19), and its inoc-
ulation in soybean is reported to improve shoot biomass, leaf
ultrastructure, and photosynthetic pigment under heat stress.
Reduction in the level of stress abscisic acid as well as an
increment in the jasmonic acid and salicylic acid content in
the rhizosphere were also observed (Kang et al. 2019). Recent
advances in the field of biofertilizers have discovered novel
elite strains like Pseudomonas plecoglossicida isolated from
soybean rhizosphere, which solubilized 75.39 mg L− 1 phos-
phorus and also produced plant growth hormones like indole
acetic acid up to 38.89 ppm (Astriani et al. 2020). Gordonia
terrae has recently been discovered to solubilize phosphorus
up to 299.3 mg L− 1 under highly saline conditions, i.e., 1.5 M
NaCl concentration (Jiang et al. 2020). Trichoderma
harzianum is also reported to solubilize phosphorus up to
288.18 μg mL− 1. The strain produced indole acetic acid
(21.14 μg mL− 1). Improved shoot and root biomass, leaf area,
and leaf numbers were observed in Solanum lycopersicum L.
plants treated with fungi, compared to uninoculated plants
(Bader et al. 2020). Many novel microorganisms are recently
reported as listed above which can solubilize phosphorus to a
wide range and produce phytohormones. The bacterial hor-
mone like indole acetic acid also suppresses the growth of
fungal pathogens by interacting with the host defense system
(Linu et al. 2019). Taken together, these findings indicate that
these microorganisms can be utilized for phosphorus balance
and overall development in plants.
One of the notable attributes of PSMs is the production of
the ACC deaminase enzyme which reduces the ethylene levels
in plants in the stress environment. Ethylene is produced in
higher amounts (large peak) > 25 μg L− 1 in stress conditions,
which retards the overall growth of plants (Gamalero and
Glick 2015). ACC deaminase transforms ACC (ethylene pre-
cursor) to α-ketobutyrate and ammonia, thereby decreasing
high ethylene levels in plants and promoting the survival
and growth of plants under stress conditions (Olanrewaju
et al. 2017). ACC deaminase producing PSMs bind to the
roots, seeds, leaves, and stem of plants that exude plant
ACC (Penrose et al. 2001), which is taken up by the bacteria
associated with plant tissue and is cleaved by ACC deaminase
(Penrose and Glick 2003). The end product of the subsequent
reaction (ammonia) is utilized by bacteria as a nitrogen source
for their growth, thereby reducing the impact of stress ethyl-
ene levels in plants (Sun et al. 2009). Interaction of plant and
ACC deaminase producing PSMs induces morphological al-
teration in plants, such as increment in root length and bio-
mass, coupled with auxin production by PSMs that promotes
plant growth. Stress induces ACC oxidase and ACC synthase
activity in plants that first leads to a small peak of ethylene (~
10 μg L− 1), which induces transcription of defense genes in
plants, and subsequently to a large deleterious ethylene peak
(> 25 μg L− 1) (Glick et al. 2007). Simultaneously, bacterial
ACC deaminase is activated due to the production of a large
amount of ACC through ACC synthase. ACC deaminase has
a lower affinity for ACC than ACC oxidase, and therefore,
PSMs with ACC deaminase activity function actively before
the induction of an appropriate amount of ACC oxidase. In
this manner, ACC deaminase reduces the high ethylene peak
(by 50–90%) and promotes plant growth under environmental
stress (Glick 2014). Phosphorus-solubilizing and ACC
deaminase-producing novel strain Bacillus subtilis Rhizo
SF48 was seen to encourage tomato plant growth under
J Soil Sci Plant Nutr
drought by improving catalase and superoxide dismutase con-
tent in bacteria-treated plants. Seed germination rate and seed-
ling vigor index also improved in inoculated plants.
Furthermore, qRT-PCR studies revealed the downregulation
of drought-responsive factor (Le25) by 0.75-fold and
ethylene-responsive factor (SlERF84) by 0.86-fold in treated
plants. The researchers concluded that this novel strain
shielded tomato plants against oxidative damage due to
drought stress and improved plant growth (Gowtham et al.
2020). These reports indicate that ACC deaminase-positive
PSMs are a boon to agriculture as they enhance the tolerance
of plants to severe stress conditions and augments the agricul-
tural productivity.
Plant-growth-promoting PSMs control plant diseases
caused by pathogens through various mechanisms like com-
petitive root colonization, synthesis of lytic enzymes and
allelochemicals, and detoxification of virulence factors and
induce systemic resistance against plant pathogens
(Compant et al. 2005; Paul and Sinha 2017). Many
phosphate-solubilizing genera like Pseudomonas, Serratia,
Bacillus, and Streptomyces secrete antifungal metabolites like
viscosinamide, peptaibols, daucans, gliovirin, terpenoids,
polyketides, pyrrolnitrin, and phenazines that downregulate
pathogenesis in the host plant (Myo et al. 2019). Another
study unveiled that Pseudomonas putida PSDM3,
Enterobacter hormaechei PSDM10, and Advenella sp.
PSDM17 isolated from treated water were capable of phos-
phorus solubilization and inhibiting Fusarium sp. infection in
wheat seedlings. These were potent fungicides (Przemieniecki
et al. 2019). Mohammed et al. (2020) discerned that
phosphate-solubilizing Pseudomonas fluorescens act as a bio-
control tool against tomato bacterial wilt causing organism
Ralstonia solanacearum. These biocontrol agents produce li-
pases, proteases, and α-amylase enzymes that act against
pathogens’ metabolic machinery, and such bacterially treated
plants displayed a low incidence of wilt and improved growth
and development. Pathogens are a major threat to plant health
as they decrease agricultural productivity and degrade the
food quality. PSMs with biocontrol activity have emerged as
a potential tool for decreasing pathogen infestation in crops in
an eco-friendly manner and are an efficient substitute for syn-
thetic chemicals used for controlling phytopathogens.
Many microbial strains can remediate toxic compounds
from the environment, such as xenobiotics, pesticides,
heavy metals, herbicides, and organic solvents, which are
poisonous for soil, plants, humans, and animals.
Phosphate-solubilizing Bacillus subtilis MF497446 can
tolerate cadmium levels up to 18 mg L− 1 and lowers the
cadmium uptake in cowpea by 29.2%. The strain also im-
proved the germination rate and seedling vigor index in
inoculated seeds under cadmium stress (up to 9 mg kg− 1)
(El-Nahrawy et al. 2019). Remediation of heavy metal con-
taminated soil through PSMs is a viable and inexpensive
strategy. These PSMs not only improve the heavy metal
tolerance of host plants but also enhance the
phytoremediation efficiency of host plants in contaminated
soil. Therefore, for remediation of toxic soil at a large
scale, optimum utilization of PSMs and plant interaction
should be encouraged.
Many studies have reported that the application of
PSMs in combination with different phosphorus sources
and nutrients (iron, silicon) improves phosphorus uptake
and phosphorus use efficiency of the crop, while also
enhancing the growth and yield of the crop. For instance,
phosphorus-solubilizing strains Pseudomonas mallei and
Pseudomonas cepaceae in combination with nano-
phosphorus (0.1 g L− 1) improved growth, yield, photo-
synthetic efficiency, chlorophyll content, and antioxidant
enzyme activity, viz., catalase, glutathione reductase, pro-
line dehydrogenase, glutathione-S-transferase, superoxide
dismutase, and ascorbate peroxidase, of Phaseolus
vu lg aris in ca lcareo us soil (Rady et al. 201 9).
Boroumand et al. (2020) reported that phosphate-
solubilizing Pseudomonas stutzeri and Mesorhizobium
sp. along with nano-silica (0.05, 0.07 ppm) improved veg-
etative growth of land cress plant, with an increment in
soil nitrogen and phosphorus content. Application of Fe-
EDTA with phosphate solubilizers Pseudomonas putida
P159, Pseudomonas fluorescens T17-24, and Bacillus
subtilis P96 improved root shoot biomass, yield, and nu-
trition of Sorghum bicolor in low fertility calcareous soil
(Abbaszadeh-Dahaji et al. 2020). Newly isolated strain
Serratia plymuthic BMA1 solubilized 450 mg L− 1 phos-
phorus and improved dry weight by 76% in inoculated
Vicia faba L. plants, compared to uninoculated plants.
The phosphorus content in roots and shoots was threefold
higher in treated plants in comparison to control plants
(Borgi et al. 2020). The consortium of phosphobacteria
(Klebsiella sp. RC3, Stenotrophomonas sp. RC5,
Klebsiella sp. RCJ4, Serratia sp. RCJ6, and
Enterobacter sp. RJAL6) with phosphorus fertilization
improved phosphorus content in the shoot of Lolium
perenne by 29.8% compared to uninoculated control, in
phosphorus-deficient soil (Barra et al. 2019). Murgese
et al. (2020) observed a significant yield increment of
49.18% in Cucumis melo L. when seeds were inoculated
with a consortium of PSMs (Enterobacter asburiae
TFD26, Pseudomonas koreensis TFD26, and
Pseudomonas linii BFS112). Such discoveries suggest
that PSMs not only improve phosphorus content in plants
but also upgrade the overall growth and health of plants,
under both normal and stress conditions. Given these
facts, PSMs are required to be further explored for their
application in conventional agriculture systems to im-
prove soil health and crop yield without hampering the
ecosystem.

4 Mechanism of Phosphorus Solubilization
by PSMs
Phosphorus dynamics in soil depends on (a) dissolution and
precipitation, (b) sorption and desorption, and (c) inter-
conversion between organic and inorganic forms of phospho-
rus (Sims and Pierzynski 2005). Mineralization, solubiliza-
tion, and immobilization are the predominant ways of dissem-
ination of phosphorus in soil by PSMs, which are influenced
by available inorganic minerals in the soil. Major strategies
adopted by PSMs for dissolution of phosphates include (a)
exudation of organic acids, protons, and siderophores; (b) ex-
cretion of extracellular enzymes; and (c) degradation of the
substrate via mineralization, as presented in Fig. 2.
4.1 Inorganic Phosphate Solubilization
Inorganic phosphates like Fe–P, Al–P, and Ca–P in the soil
are solubilized in the following ways.
4.1.1 Production of Organic Acids
Organic acids like citric acid, gluconic acid, oxalic acid, and
tartaric acid exuded by PSMs solubilize inorganic phosphates
by (a) chelation of cations bound to phosphate, (b) reducing
pH, (c) complexation with metal ions bound to phosphates,
and (d) challenging P for adsorption site (Kishore et al. 2015).
Organic acids are low molecular weight compounds that che-
late the phosphorus-bound cation through their hydroxyl and
carboxyl groups and lower the rhizospheric pH through the
gaseous exchange (O2/CO2) and proton-bicarbonate balance,
thereby releasing the bound phosphorus (Kim et al. 1997).
Fermentation, respiration of organic carbon compounds, or
Fig. 2 Schematic presentation of
phosphate solubilization by
phosphate-solubilizing
microorganisms. (PSB plate
shown in the figure represents the
phosphate-solubilizing bacteria
with halo zone formation. PSB
was isolated by the author and
inoculated in Pikovskaya agar
having tricalcium phosphate. A
clear zone formed by the bacteria
indicates the solubilization of
tricalcium phosphate. Halo zone
experiment is performed for the
qualitative screening of
phosphate-solubilizing
microorganisms). P phosphorus,
PSB phosphate-solubilizing
bacteria, H2S hydrogen sulfide,
CP carbon-phosphorus
J Soil Sci Plant Nutr
direct oxidation are key metabolic pathways for organic acid
production by PSMs that result in acidification in the vicinity
of microbes, liberating phosphates from complexes by substi-
tution of protons for cations like Fe+3 and Al+3 (Goldstein
1994), or by the exchange of phosphate (PO42−) by acidic
anions. 2-Ketogluconic acid and gluconic acid are major acids
excreted by PSMs (Duebel et al. 2000). Secretion of gluconic
acid by PSMs is mediated by glucose dehydrogenase enzyme
(a quinoprotein) in the direct oxidation pathway of glucose.
Glucose dehydrogenase enzyme is encoded by the glucose
dehydrogenase (gcd) gene and has pyrroloquinoline quinone
(PQQ) as a cofactor. PQQ is a redox-active molecule encoded
by pqq operon that consists of the core genes pqq A, B, C, D,
E, and F, which are responsible for dehydrogenase activity
and mineral phosphate solubilization in the microorganisms
(Wan et al. 2020). A previous study reported that disruption of
the pqqA gene in gram-negative Rahnella aquatilis HX2 sig-
nificantly reduced the gluconic acid content from 9.68 to
0.65 g L− 1 in the culture media. Mutation of the pqqA gene
also resulted in lower soluble phosphorus content (99.7 mg L−
1
) compared to phosphorus content (465.9 mg L− 1) of the
wild-type strain (Li et al. 2014). Many studies have shown
that inorganic phosphate solubilization abilities of bacteria
and fungi depend on the pqq gene (Chen et al. 2016; Otieno
et al. 2015; Suleman et al. 2018). Predominant organic acids
secreted by PSMs as a major mode of phosphorus dissolution
are listed in Table 5. Phosphorus-solubilizing Pseudomonas
sp. strain AZ15 produced oxalic acid, gluconic acid, acetic
acid, lactic acid, and citric acid and solubilized phosphorus
up to 109.4 μg mL− 1. Moreover, this strain also enhanced
yield attributes like dry matter accumulation, grain yield,
number of nodules, and nodule dry weight in chickpea
(Zaheer et al. 2019). It was evident from the findings that
J Soil Sci Plant Nutr

Table 5 Principle organic acids produced by phosphate-solubilizing microorganisms

Phosphate-solubilizing microorganisms Organic acids References

Bacillus cereus, Bacillus subtilis, Paenibacillus sp. Oxalic acid, malic acid, formic acid, acetic Chawngthu et al. (2020)
acid, tartaric acid, gluconic acid
Trichoderma sp. Lactic acid, fumaric acid, ascorbic acid, Bononi et al. (2020)
isocitric acid, malic acid, citric acid, phytic acid
Pantoea agglomerans NCTC 9381, Pantoea vagans LMG 24199, Citric acid, fumaric acid, acetic acid, succinic acid, Rfaki et al. (2020)
Pseudomonas azotoformans NBRC 12693, Enterobacter gluconic acid, oxalic acid
ludwigii EN-119, Serratia quinivorans 4364
Pseudomonas, Burkholderia, Klebsiella, Achromobacter, Gluconic acid, oxalic acid, lactic acid, Nacoon et al. (2020)
Sphingobacterium acetic acid, malic acid, tartaric acid
Bacillus megaterium, Bacillus subtilis, Bacillus licheniformis Citric acid, acetic acid, propionic acid, Do carmo et al. (2019)
lactic acid
Leclercia adecarboxylata B3 Formic acid, gluconic acid, malonic acid, Teng et al. (2019b)
acetic acid, citric acid, succinic acid
Penicillium oxalicum, Aspergillus niger Oxalic acid, formic acid, tartaric acid, malic acid, Li et al. (2016)
citric acid, acetic acid
Aspergillus niger FS1, Eupenicillium ludwigii FS27, Penicillium Citric acid, gluconic acid, oxalic acid Mendes et al. (2013)
islandicum FS30, Penicillium canescens FS23
Pseudomonas poae BIHB 751 Gluconic acid, ketogluconic acid, citric acid, malic acid Vyas and Gulati (2009)
Trichoderma flavus, Trichoderma helicus, Penicillium Glucuronic acid, gluconic acid, succinic acid, butyric Scervino et al. (2010)
purpurogenum, Penicillium janthinellum acid, valeric acid, citric acid, fumaric acid, propionic
acid, acetic acid
Acinetobacter rhizosphaerae BIHB723 Gluconic acid, formic acid, oxalic acid Gulati et al. (2010)
Pseudomonas trivalis BIHB 769 Gluconic acid, ketogluconic acid, lactic acid, fumaric Vyas and Gulati (2009)
acid, malic acid, succinic acid
Arthrobacter Hy-505 Oxalic acid, gluconic acid, lactic acid, citric acid Yi et al. (2008)
Pseudomonas corrugata NRRLB-30409 2-Ketogluconic acid Trivedi and Sa (2008)
Bacillus megaterium CC-BC10, Serratia marcescens CC-BC03 Citric acid, lactic acid, propionic acid, gluconic acid Chen et al. (2006)

phosphorus-solubilizing Trichoderma strains (AMS 34.39,
AMS 31.15, and AMS 1.43) produced different organic acids
like ascorbic acid, citric acid, malic acid, gluconic acid, and
phytic acid as the major mode for phosphorus solubilization in
soybean. In addition, these novel strains improved plant
growth from 2.1 to 41.4% in comparison to untreated plants
(Bononi et al. 2020).
Several mechanisms are adopted by PSMs for the dissolu-
tion of phosphorus, although the dominant one was found to
be the acidification of the surroundings by the production of
organic acids. These mechanisms need to be explored in great-
er detail for a better understanding of the microbial action for
phosphorus dissolution (Ameen et al. 2019).
4.1.2 Inorganic Acid and H2S Production
Hydrochloric acid, sulfuric acid, nitric acid, and carbonic acid
production by PSMs have been reported to solubilize phos-
phate, but with low efficiency compared to organic acids. The
mechanism of production of inorganic acids like nitric acid
and sulfuric acid is adopted by Nitrobacter and Thiobacillus
spp., respectively, to dissolve phosphorus (Shrivastava et al.
2018). Kim et al. (1997) reported the dissolution of phospho-
rus by HCl by reducing pH to the same level as organic acids,
but with lower efficiency. Acidophilic and sulfur-oxidizing
bacteria produce H2S as a metabolic byproduct of microbial
decomposition of organic matter, sulfate reduction, and other
biochemical reactions, which reacts with ferric phosphate and
forms ferrous sulfate, releasing the bound phosphorus
(Florentino et al. 2016). It was observed that sulfur-
oxidizing bacteria Delftia sp. strain SR4 oxidized 1 g L− 1
elemental sulfur to 203 mg L− 1 sulfate and 20 mM thiosulfate
to 220 mg L−1 sulfate. This strain exhibited up to 116% higher
phosphorus-solubilizing efficiency in inoculated plants of
Brassica juncea, in comparison to uninoculated plants (Roy
and Roy 2019).
4.1.3 Proton Release from NH4+ (Assimilation/Respiration)
Proton extrusion is an alternative mode of phosphorus disso-
lution in soil by microorganisms (Parks et al. 1990). Analysis
of culture filtrate of Pseudomonas sp. found phosphorus dis-
solution activity, but no organic acid production (Illmer and
Schinner 1995). Ammonium (NH4+) present in soil is assim-
ilated by PSMs for synthesis of amino acids. Inside the micro-
bial cell, NH4+ is converted to ammonia (NH3) and the excess
proton H+ is released into the cytoplasm of the microbial cell.
This acidifies the medium surrounding the microbial cell,

which aids in dissolution of insoluble phosphates (Gaind
2016). Proton excretion lowers the soil pH and is dependent
on the nitrogen source used. Sharan and Darmwal (2008) pro-
vided evidence that the amount of P dissolved was high when
NH4+ was used as a nitrogen source, compared to NO3−. This
phenomenon of phosphorus dissolution is predominant in
some microbes only, indicating the prevalence of diverse
modes of phosphorus solubilization, as proton extrusion is
achieved by other modes also, as revealed from the work of
Park et al. (2009) and Reyes et al. (1999). Proton exclusion
theory of phosphate dissolution was studied in alkalophilic
Bacillus marisflavi FA7. Maximum tricalcium phosphate dis-
solution by the strain was observed when NH4Cl was supple-
mented in the media as an inorganic nitrogen source (Prabhu
et al. 2018). A multifunctional Bacillus subtilis BPM12 strain
was reported to solubilize maximum phosphorus
(272.02 μg m L−1) in vitro when media was supplemented
with (NH4)2SO4 as a nitrogen source (Wang et al. 2020).
4.1.4 Indirect Mechanism
Rhizospheric microbes assimilate a large amount of phospho-
rus indirectly from the soil, dissolving insoluble phosphorus
(Halvorson et al. 1990). Microbial cell lysis during stress con-
ditions releases this phosphorus into the soil, which is taken up
by plants and other soil organisms (Butterly et al. 2009).
Investigation showed that soil drying with subsequent fumi-
gation for a varied number of days, i.e., for 2 and 14 days at
40 °C resulted in a decline in microbial biomass phosphorus
by 61 and 70%, respectively. This finding proposed the cor-
relation between soil drying, the mortality of microbial cells,
and microbial biomass phosphorus, indicating the indirect
mode of microbial contribution to available phosphorus in soil
(Khan et al. 2019b).
4.1.5 Direct Oxidation Pathway
Extracellular oxidation pathway by microbes dissolves insol-
uble phosphates present in the soil, as proposed by Goldstein
(1995). In the direct oxidation pathway, glucose is converted
to gluconic acid by glucose dehydrogenase and further oxi-
dized to 2-ketogluconic acid by gluconate dehydrogenase.
These acids act as chelators of minerals like Ca2+ and Fe2+
from their phosphate-bound form (Krishnaraj and Goldstein
2001). This was evidenced by Song et al. (2008) while study-
ing insoluble phosphorus dissolution by Burkholderia cepacia
DA23. This mode of phosphorus dissolution is predominant
in gram-negative bacteria, where dominant organic acids like
gluconic acid are produced via alternate pathways for glucose
oxidation and diffuse through bacterial periplasm into the sur-
roundings (Krishnaraj and Dahale 2014). Pseudomonas
aeruginosa KR270346 also solubilizes phosphorus by
J Soil Sci Plant Nutr
secreting gluconic acid by direct oxidation pathway as the
dominant acid for phosphorus solubilization (Linu et al.
2019).
4.1.6 Exopolysaccharide (EPS) Production
Exopolysaccharides are homo or heteropolymers of carbohy-
drates with an organic or inorganic component that is exuded
by microorganisms outside their cell wall (Sutherland 2001).
EPS is produced by microbes in response to stress or biofilm
formation. EPS forms complexes with metal ions present in
soil (Al3+>Cu2+>Zn2+>Fe3+>Mg2+>K+) (Ochoa-Loza et al.
2001), and this mechanism can be extrapolated as a means
of P solubilization by EPS-secreting microorganisms. Yi
et al. (2008) investigated the ability of tricalcium phosphate
dissolution of four phosphorus-solubilizing bacterial strains,
i.e., Enterobacter sp. (EnHy-401), Azotobacter sp. (AzHy-
510), Arthrobacter sp. (ArHy-505), and Enterobacter sp.
(EnHy-402), and concluded that the concentration of EPS
and microbial origin were responsible for solubilization
(Kishore et al. 2015). EPS production by soil microflora is
also enhanced under stress conditions, as evident from the
study of Silambarasan et al. (2019). Therefore, EPS produc-
tion by microbes functions as a shield against stress in plants.
In the strain Paenibacillus polymyxa GOL 0202, EPS produc-
tion was evident along with phosphate solubilization efficien-
cy. The strain also improved the germination rate and root and
shoot length in wheat seedling (Cherchali et al. 2019).
4.1.7 Siderophore Production
Siderophores are low molecular weight high-affinity iron-
chelating compounds that are excreted by microorganisms
and plants in response to iron stress in the environment.
These are the strongest ferric ion complexing agents
(Birch and Bachofen 1990). Currently, more than 500
siderophores are known that are produced by both plants
and microbes (Sharma et al. 2013). PSMs also release
siderophores as a strategy to chelate iron from Fe–P com-
plexes in the soil (Collavino et al. 2010), although its role in
phosphate dissolution needs to be further investigated. It
was reported that under alkaline conditions, several phos-
phate solubilizers like Bacillus megaterium, Bacillus
subtilis, Rhizobium radiobacter, and Pantoea allii pro-
duced siderophores in the range of 80 to 140 μmol L− 1,
which encouraged the survival of organisms under stress
environment and also improved phosphorus solubilization
(Ferreira et al. 2019). Toscano-Verduzco et al. (2020) found
that novel fungi Beauveria brongniartii secreted
siderophores, i.e., 59.8% of Fe3+-Chrome azurol-S degra-
dation, and solubilized 158.95 mg L− 1 phosphorus in vitro.
J Soil Sci Plant Nutr
4.2 Organic Phosphate Solubilization
Organic phosphates constitute 20–30% of the total phospho-
rus in soil. The dissolution of organic phosphates occurs via
the mineralization process through the action of enzymes
(Kumar and Shastri 2017).
(a) Non-specific acid phosphatases (NSAPs)
(b) Phytases
(c) Phosphonatases and C–P lyases
4.2.1 Non-Specific Acid Phosphatases (NSAPs)
NSAPs are also known as phosphomonoesterases and are of
two types: acid and alkaline phosphatases that are secreted by
PSMs (Nannipieri et al. 2011). These enzymes are categorized
based on pH optima. Acid phosphatases prevail in acidic soil
and alkaline phosphatases in alkaline to neutral soil (Eivazi
and Tabatabai 1977; Renella et al. 2006). Dephosphorylation
of phosphoesters or phosphoanhydride bonds of organic com-
pounds is catalyzed by phosphatases. It has been evidenced
that both acid and alkaline phosphatases are excreted by mi-
croorganisms which have greater affinity to organic phospha-
tases in soil (Sharma et al. 2013; Tarafdar et al. 2001). Also,
alkaline phosphatases hydrolyze about 90% of total organic
phosphorus in soil and make phosphorus available to plants
(Jarosch et al. 2015). It was seen that purified alkaline phos-
phatases from Bacillus licheniformis MTCC 2312, when in-
oculated in soil, improved percentage phosphorus content in
the root and stem of Zea mays L. by 2.35- and 1.76-fold,
respectively (Singh and Banik 2019). Coinoculation in soil
of phosphate-solubilizing fungus Talaromyces helices L7B
and arbuscular mycorrhizal fungus Rhizophagus irregularis
enhanced soil alkaline phosphatase activity (459.38 EU) com-
pared to uninoculated soil (47.86 EU) and also improved soil
soluble phosphorus by 50% compared with control (Della
Monica et al. 2020).
4.2.2 Phytases
Phytases catalyze the removal of phosphorus from the phytate
compound (abundant organic phosphorus in soil), which is the
dominant source of inositol and stored phosphorus in seeds
and pollen (Sharma et al. 2013). The potential of plants to
obtain phosphorus from phytate is very limited. Research
showed that microbes play a significant role in the minerali-
zation of phytate; when Arabidopsis plant was genetically
transformed with the phyA gene from Aspergillus niger, phos-
phorus nutrition and growth improved in the transformed
plant (Richardson 2001). Inoculation with phytase-
producing bacteria in cereal crops resulted in enhanced phos-
phorus uptake without the use of fertilizer (Martinez et al.
2015). Phosphate-solubilizing fungi Aspergillus niger pro-
duced maximum phytase (133 IU) and phosphatase (170 IU)
in 48 h of solid-state fermentation and solubilized phosphorus
up to 835 ppm. Field trial studies showed that the fungus strain
improved plant height, leaf length, and fruit number per plant
in Lagenaria siceraria and Abelmoschus esculentus when
compared with uninoculated plants (Din et al. 2019). Elite
strains Pseudomonas corrugata SP77 and Serratia
liquefaciens LR88 were studied for phytase production and
were both found to display phytase activity up to 23.02 and
24.84 U mL− 1, respectively, with improved phosphorus sol-
ubilization efficiency up to 714.96 and 306.74 μg mL− 1, re-
spectively (Ben Zineb et al. 2020).
4.2.3 Phosphonatases/Carbon–Phosphorus (C–P) Lyases
This class of enzymes catalyzes the cleavage of the C–P bond
of organophosphates, improving the phosphorus availability
to plants (Rodriguez et al. 2006). There is not much evidence
of significant organic phosphorus solubilization through ly-
ases, as their activity is low because of the low availability
of their substrates in the soil (Selvapandiyan and Bhatnagar
1994). CP lyases’ activity is reported in many phosphate-
solubilizing bacteria like Bacillus, Pseudomonas,
Enterobacter, Acinetobacter, Rhizobium, and Burkholderia
(Teng et al. 2019a; Vazquez et al. 2000) and in endophytic
fungi like Aspergillus, Penicillium, Piriformospora, and
Curvularia (Mehta et al. 2019).
5 Molecular Aspects of Phosphate
Solubilization by PSMs
Genetic studies on phosphate solubilization are sparse and
reveal that only a few genes control the action of phosphate
dissolution. These genes include pyrroloquinoline quinine
genes (pqq A, B, C, D, E, F) that code for PQQ—a small,
redox-active molecule and a cofactor for glucose dehydroge-
nase that catalyzes the conversion of glucose to gluconic acid
which is the principal organic acid produced by PSMs for
dissolution of phosphorus (Kumar and Shastri 2017). These
genes can be isolated and cloned to other soil microorganisms
for enhancing their phosphorus-solubilizing ability (Babu-
Khan et al. 1995; Ludueña et al. 2017). For instance,
rhizobium can be transformed by pqq genes that can improve
their nitrogen-fixing as well as phosphate-solubilizing capa-
bility. The transformation of phosphate-solubilizing genes in-
to microbes helps avoid the requirement of using consortia for
the same purpose (Sharma et al. 2013). Mineral phosphate-
solubilizing genes (mps) were also isolated from Erwinia
herbicola that codes for gluconic acid production and dis-
solves mineral phosphorus in E. coli HB101 (Goldstein and
Liu 1987; Rodrıguez et al. 2000). Another mineral phosphate

solubilization gab Y gene was isolated from Burkholderia
cepacia that expressed an apo glucose dehydrogenase for
gluconic acid production, which solubilizes inorganic phos-
phorus (Zhao et al. 2014). Bacterial phosphatases are the nov-
el enzymes involved in hydrolysis of labile
phosphomonoesters to orthophoshates. The quantification of
functional genes indicates the biological reactions involved in
phosphorus turnover. Quantification of the bacterial phospha-
tase gene (phoC and phoD) abundance in soil was performed
through quantitative real-time PCR. A positive correlation
was observed between phosphatase gene abundance in soil,
phosphatase activity in rhizosphere, and plant phosphorus up-
take, indicating the significance of bacterial genes for phos-
phorus turnover in soil (Fraser et al. 2017). Acid phosphatase
genes (acp) expressing acid phosphatase activity with broad
substrate range were isolated Burkholderia pyrrocinia (Zhu
et al. 2019), and non-specific acid phosphatase genes (phoC
and napA) were isolated from Morganella morganii for or-
ganic phosphorus solubilization (Thaller et al. 1994;
Rodriguez et al. 2006). Recent studies have also unveiled a
novel glucose dehydrogenase gene (gcd) and an enolase gene
(eno) that are responsible for phosphorus solubilization. The
gcd genes mediate gluconic acid formation, which is a major
mode for phosphate solubilization. Acinetobacter sp. MR5
(DSM 106631) and Pseudomonas sp. MR7 (DSM 106634)
with gcd gene enhanced phosphorus biofortification and plant
growth promotion in rice. About 67% increment in plant
phosphorus content and 55% in grain yield was notable in
bacterially treated rice plants, compared to control plants with
a 20% decrement in fertilizer input (Rasul et al. 2019). Zhang
et al. (2018) reported that the hyphal exudates of arbuscular
mycorrhizal fungus Rhizophagus irregularis MUCL 43194
induce the expression of the phosphatase gene in phosphate-
solubilizing bacteria Rahnella aquatilis HX2. The expression
of phosphorus cycling genes (pqqC, phoX, phoD, bbb) of
bacterial c ommunities ( Burkholderia, N i a s t e l l a,
Paenibacillus, Lysobacter, Agromyces, Pseudomonas,
Pedobacter, and Bacillus) in proximity with the Penicillium
hyphae was high in comparison to native soil inhabitants (Hao
et al. 2020). Fungi therefore indirectly enhance the
phosphorus-solubilizing potential of closely associated bacte-
ria. It was in Burkholderia cepacia strain 71-2 that it was first
reported that the eno gene (encoding enolase in E. coli) was
responsible for phosphorus solubilization (Liu et al. 2019a).
An artificial biological approach was used to engineer
rhizospheric bacteria Pseudomonas simiae WCS417r,
Ralstonia sp. strain UNC404CL21Col, and Pseudomonas
putida KT2440 with distinct phytase genes, and such
engineered strains released greater amount of inorganic phos-
phorus (˃ 500 μM) from phytate in liquid culture media as
compared to strains without phytase genes, which released
only 5–8 μM phosphorus from phytate (Shulse et al. 2019).
J Soil Sci Plant Nutr
There are novel molecular approaches for screening of
PSMs and genes related to phosphate solubilization. DNA
reassociation technique is an important molecular tool to make
comparisons and calculate similarities between genomes of
different microorganisms. Genetic similarity of diverse
PSMs is studied using this method (Kumar et al. 2019;
Mahato et al. 2017). Fatty acid methyl esters (FAME) analysis
method is used for identification and determination of species.
This method is based on the profiling of fatty acid methyl
esters, which is specific for different species of microorgan-
isms (Alaylar et al. 2020). Novel PSMs have been identified
from natural ecosystems using this technique (Chen and Liu
2019). Denaturing gradient gel electrophoresis (DGGE) is an
intermediate resolution method. DNA is isolated from soil
samples and subjected to real time polymerase chain reaction
with primers for specific markers (16S rRNA and 18S rRNA).
The PCR amplicons are separated in gradient gels (formamide
and urea) according to melting behavior of DNA. DGGE pro-
file reflects the diversity and richness of the microbial com-
munity in environmental samples (Alaylar et al. 2020). The
diversity of PSMs in soil samples can be analyzed by this
molecular approach. DGGE analysis of DNA extracted from
kitchen waste during composting revealed that inoculation of
enriched PSB into the kitchen waste compost changed the
bacterial diversity and community, which improved the phos-
phorus solubilization process and organic acid production
(Wei et al. 2018). The diversity in bacterial community struc-
ture of soil from extreme environment of Chile was studied
through DGGE. It was revealed that bacterial phosphatase
genes were abundantly present in the extreme environment
and were positively correlated to phosphatase enzyme activity
in soil (Acuña et al. 2016). Novel proteomics techniques are
also utilized for identification of PSMs and proteins involved
in phosphorus solubilization. The phosphorus-solubilizing po-
tential of Pseudomonas putida BIRD-1, Pseudomonas
fluorescens SBW25, and Pseudomonas stutzeri DSM4166
was examined through the proteomics approach, in response
to phosphorus deficiency. Exoproteomic analysis of
Pseudomonas strains revealed the expression of four different
phosphate-binding proteins, glucose dehydrogenase protein,
and phosphatase protein in phosphorus-starved cells of bacte-
ria (Lidbury et al. 2016). Whole-genome shotgun sequencing
is a novel metagenomics approach used widely for sequencing
of the entire genome. It is based on DNA fragmentation and
assembly of fragments through overlapping ends
(Bergkemper et al. 2016b). This approach was utilized by
Bergkemper et al. (2016a) to study the diversity of soil mi-
crobes responsible for phosphorus turnover in soil. Novel ol-
igonucleotide primers encoding the phosphate-solubilizing
genes (phoD, phoN, appA, gcd, and phonX) were synthesized
for amplification of the target genes from diverse soil micro-
organisms. Next-generation sequencing of the desired
J Soil Sci Plant Nutr
amplicons was carried out, and microbial diversity responsible
for phosphorus turnover in soil was identified. gcd primers
amplified the target gene from different phyla, viz.,
Burkholderiales, Rhizobiales, and Rhodospirillales.
Similarly, PhonX primers amplified the gene from
Proteobacteria and Fermicutes. phoD primers also amplified
the gene from phyla Pseudomonadales, Actinomycetales,
Rhizobiales, and Burkholderiales. This study focused on the
application of novel primers for the identification of microbial
diversity in soil that drives the phosphorus pool in soil. Such
findings focus on the development of genomic and proteomic
tools for detection of novel PSMs and improving their multi-
ple plant-growth-promoting attributes, as these omic ap-
proaches are rapid, reliable, and sensitive compared to
culture-dependent techniques.
6 Conclusion
Global crop production in the world is limited by phos-
phorus nutrition. To overcome the problem of phosphorus
unavailability in agricultural soil, phosphatic fertilizers are
frequently applied in an unbalanced manner which de-
grades the soil and crop health. Application of
phosphate-solubilizing microorganisms (PSMs) in the soil
is therefore a promising approach without negative envi-
ronmental and socio-economic consequences. These mi-
croorganisms solubilize the unavailable phosphorus in
soil and also restores the nutritional status of soil through
diverse mechanisms as discussed in the review. Combined
supplementation of PSMs and rock phosphates in the ag-
ricultural field is another option to improve the phospho-
rus use efficiency and yield of the crop. Many novel
PSMs are discovered in recent years which are versatile
in their functions in normal and stressed environment.
However, selection of a potent phosphate solubilizer with
multifunctional plant-growth-promoting traits is of utmost
i m p or t a nc e f o r the d ev el o pm e nt of c om m er c i al
biofertilizers with longer shelf life. Conclusively, there
is a need for additional research to discover new isolates
from diverse ecological niches and to further explore their
metabolism for improving their phosphate-solubilizing ca-
pability. Metagenomics approach should also be encour-
aged to modify not only PSMs but also other microorgan-
isms for improving and introducing phosphate-
solubilizing efficiency.
Acknowledgments This manuscript preparation did not receive any spe-
cific grant from funding agencies in the public, commercial, or profit
sectors.
Availability of Data and Materials The authors declare that all the figures
and tables presented in this manuscript are original and if taken from other
papers are properly cited.
Compliance with Ethical Standards
Conflict of Interest The authors declare that they have no conflict of
interest.
Ethical Approval Not applicable for this manuscript
Consent to participate All the co-authors have participated in the prep-
aration of this manuscript as per the requirement.
Consent for Publication All the co-authors have already given their
consent for publication of this manuscript.
Code Availability Not applicable
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