Pedosphere 31(1): 43–75, 2021

doi:10.1016/S1002-0160(20)60057-1
ISSN 1002-0160/CN 32-1315/P
© 2021 Soil Science Society of China
Published by Elsevier B.V. and Science Press

Biodiversity, current developments and potential biotechnological applications of

phosphorus-solubilizing and -mobilizing microbes: A review

Divjot KOUR1 , Kusam Lata RANA1 , Tanvir KAUR1 , Neelam YADAV2 , Ajar Nath YADAV1,∗ , Manish KUMAR3 ,
Vinod KUMAR4 , Harcharan Singh DHALIWAL1 and Anil Kumar SAXENA5
1 Department of Biotechnology, Dr. Khem Singh Gill Akal College of Agriculture, Eternal University, Baru Sahib, Sirmour 173101 (India)
2 Gopi Nath P.G. College, Veer Bahadur Singh Purvanchal University, Ghazipur 275201 (India)
3 Amity Institute of Biotechnology, Amity University, Gwalior 474005 (India)
4 Biochemistry, Forage Section, College of Agriculture, CCS Agricultural University, Haryana 125004 (India)
5 ICAR-National Bureau of Agriculturally Important Microorganisms, Kusmaur 275103 (India)

(Received November 4, 2019; revised December 30, 2019)

ABSTRACT
As one of the most important and essential macronutrients next to nitrogen, phosphorus (P) is important for plant development, but it is the least mobile
nutrient element in plant and soil. Globally, P is mined from geological sediments and added to agricultural soils so as to meet the critical requirements of
crop plants for agronomic productivity. Phosphorus exists in soil in both organic and inorganic forms. The various inorganic forms of the element in soil are
salts with calcium, iron, and aluminum, whereas the organic forms come from decaying vegetation and microbial residue. There is a huge diversity of plant
microbiomes (epiphytic, endophytic, and rhizospheric) and soil microbiomes that have the capability to solubilize the insoluble P and make it available to plant.
The main mechanism for the solubilization of inorganic P is by the production of organic acids, which lowers soil pH, or by the production of acid and alkaline
phosphatases, which causes the mineralization of organic P. The P-solubilizing and -mobilizing microorganisms belong to all three domains, comprising
archaea, bacteria, and eukarya. The strains belonging to the genera Arthrobacter, Bacillus, Burkholderia, Natrinema, Pseudomonas, Rhizobium, and Serratia
have been reported as efficient and potential P solubilizers. The use of P solubilizers, alone or in combination with other plant growth-promoting microbes as
an eco-friendly microbial consortium, could increase the P uptake of crops, increasing their yields for agricultural and environmental sustainability.
Key Words: crop improvement, gene expression, microbial diversity, organic acid production, P mineralization, P solubilizer, phosphatase production, plant
growth-promoting traits

Citation: Kour D, Rana K L, Kaur T, Yadav N, Yadav A N, Kumar M, Kumar V, Dhaliwal H S, Saxena A K. 2021. Biodiversity, current developments and
potential biotechnological applications of phosphorus-solubilizing and -mobilizing microbes: A review. Pedosphere. 31(1): 43–75.

INTRODUCTION 2015; Jha et al., 2018) and found in higher concentrations in

The most vital macroelements required for plant growth
is phosphorus (P), which builds up about 0.2% of plants on
a dry weight basis. It is known to have both structural and
metabolic functions in plants. It is a constituent of the nucleic
acids and phospholipids present in biomembrane, and it is
involved in the energy transfer mechanism in biological
systems. In addition, it also makes an important contribution
to seed formation, root elongation, disease tolerance, and
cold tolerance in plants. The quality of fruits, grain crops, and
vegetables is significantly influenced by the P uptake (Wiwart
et al., 2009). Although the total amount of P in the soil may
be high, it is often present in unavailable forms or in forms
that are only available outside of the rhizosphere. Mineral
forms of P include apatite, hydroxyapatite, and oxyapatite,
and their characteristic feature is that they are poorly soluble.
The organic P fraction is formed because of phosphodiesters,
phospholipids, phosphotriesters, and nucleic acids (Pii et al.,
∗ Corresponding author. E-mail: ajar@ete3rnaluniversity.edu.in, ajarbiotech@gmail.com.
fine-textured soils than in coarse-textured soils. The major
reason for P unavailability is its precipitation with various
metals such as aluminum, calcium, and iron in soil (Igual et
al., 2001).
With scientific development and modernization in agri-
cultural practices, the use of pesticides and chemical fer-
tilizers is increasing so that high yields of crops can be
obtained. The nutritional requirements of plants are easily
fulfilled by chemical fertilizers, which can provide an array
of macronutrients and micronutrients. Phosphatic fertilizers
are used in recommended doses, as excessive use will harm
the environment (Khan et al., 2007). However, the production
of chemical fertilizers is a costly and highly energy-intensive
process, requiring huge amounts of energy to meet the global
demand. Furthermore, mining rates are so high that the
depletion of the reserves will occur in about 500–600 years
(Sharma et al., 2013). Beyond this time, the processing of
44
lower grade rock will be required for the production of P-
based fertilizers (Isherwood, 2000). Thus, environmentalists
and researchers are focusing on finding alternative strategies
to address the problems associated with P solubilization in
soil (Krishnaraj and Dahale, 2014). There is a huge diversity
of P-solubilizing microbes belonging to all three domains,
comprising archaea, bacteria, and eukarya. They have the
ability to solubilize insoluble P and make it available for the
plants (Yadav et al.,2017a, 2020). Their population accounts
for 20%–40% of the total population of the rhizosphere and
about 10%–15% of the total population of the bulk soil.
Present review deals with the biodiversity of P-solubilizing
microbes, mechanisms of P solubilization and mobilization,
genes that are responsible for P solubilization and the impor-
tant role these microbes play in the crop improvement for
sustainable agriculture.
CHARACTERIZATION OF P-SOLUBILIZING MIC-
ROBES
The solubilization of insoluble P by microbes was repor-
ted by Pikovskaya (1948). There is a vast diversity of bacte-
rial, archaeal, and fungal strains with P-solubilizing capa-
bilities. They are ubiquitous, but vary in their P-solubilizing
capabilities. In soil, it has been estimated that 1%–50%
of bacteria and 0.1%–0.5% of fungi can carry out P solu-
bilization. They have been isolated from the rhizosphere,
rhizoplane, phyllosphere, rock phosphate deposit areas, and
even stressed soils and characterized using various culturable
and unculturable techniques (Wakelin et al., 2004; Zaidi
et al., 2009). Archaeal, bacterial, and fungal isolates that
exhibit P-solubilizing activities are detected by the formation
of clear halo zones, which indicate P solubilization around
the colonies (Verma et al., 2013, 2015; Yadav et al., 2017b).
However, the formation of halo zones on a solid agar medium
should not be considered the only test for assessing the P-
solubilizing capabilities of microbes; it is also important
to perform additional tests in liquid media. Furthermore,
after confirming in liquid medium, selected isolates could be
tested for the production of different organic acids. Finally,
isolates fulfilling the above-mentioned criteria should be
tested on a model plant for ultimate confirmatory test of
their P-solubilizing capability (Bashan et al., 2013). Viable
microbial preparations exhibiting P-solubilizing activity are
generally termed microphos (Zaidi et al., 2009). Factors
such as the concentration of the iron ore, temperature, and
availability of carbon and nitrogen (N) sources can affect the
P-solubilizing potential of these microbes. Ammonium salts
are known as best N sources for these microbes; other sources
include asparagine, sodium nitrate, potassium nitrate, urea,
and calcium nitrate (Ahuja et al., 2007). The P-solubilizing
microbes that show great P solubilization under in vitro
D. KOUR et al.
conditions may be selected further for bulk production so
that they can be ultimately used by farmers. For instance, the
fungi Penicillium bilaiae (Jump Start, Philom Bios, Saska-
toon, Canada) and Penicillium radicum (PR-70 RELEASE,
Bio-Care Technology, Somersby, Australia) have already
been commercially released for improving P availability to
plants (Zaidi et al., 2009). The isolation of P-solubilizing
microbes from diverse habitats, characterization of their
plant growth-promoting attributes, mechanisms of P solu-
bilization, and possible biotechnological applications for
agricultural sustainability are shown in Fig. 1.
BIODIVERSITY AND ABUNDANCE OF P-SOLU-
BILIZING MICROBES
Phosphorous-solubilizing microbes can belong to diverse
phyla, such as Actinobacteria, Ascomycota, Bacteroidetes,
Basidiomycota, Euryarchaeota, Firmicutes, Mucoromycota,
and Proteobacteria. One percent of P solubilizers belong to
Bacteroidetes, and 6% belong to Actinobacteria. The most
dominant phylum among bacteria is Proteobacteria (38%),
followed by Firmicutes (22%). Nine percent of P-solubilizing
archaea also belong to Euryarchaeota. Among P-solubilizing
fungi, the least represented phyla are Mucoromycota (1%)
and Basidiomycota (3%), whereas 20% of P-solubilizing
fungi belong to Ascomycota (Fig. 2a). In this review,
about 551 P solubilizers have been reviewed from various
sources (Table SI, see Supplementary Material for Table SI).
The most predominant genus among P-solubilizing bacte-
ria is Bacillus, followed by Pseudomonas, Acinetobacter,
Streptomyces, Burkholderia, Serratia, Enterobacter, Paeni-
bacillus, Stenotrophomonas, Staphylococcus, Arthrobac-
ter, Pantoea, Methylobacterium, Alcaligenes, Azotobac-
ter, Ochrobactrum, Rhizobium, Acetobacter, Achromobac-
ter, Brevibacterium, Brevundimonas, Klebsiella, Leclercia,
Lysinibacillus, Rhodococcus, Sphingomonas, Aeromonas,
Azospirillum, Ensifer, Exiguobacterium, Microbacterium,
Planococcus, Ustilago, and Xanthomonas. Among the P-
solubilizing fungi, most of the species belong to the genus As-
pergillus, followed by Penicillium, Fusarium, Trichoderma,
Talaromyces, Meyerozyma, Candida, Pseudozyma, Arthro-
derma, Cryptococcus, Pichia, Eupenicillium, Paecilomyces,
Rhodosporidium, Rhodotorula, Saccharomyces, and Sporidi-
obolus. However, few P-solubilizing fungal species be-
longed to Agromyces, Bradyrhizobium, Corynebacterium,
Erwinia, Herbaspirillum, Lecanicillium, Oceanobacillus,
Psychrobacter, Rhodobacter, Sinorhizobium, and Strepto-
coccus (Fig. 2b).
Furthermore, regarding the phylogenetic profiling of
P-solubilizing microbes, the most dominant phylum among
bacteria is Proteobacteria, followed by Firmicutes. Pro-
teobacteria consist of 49 diverse species belonging to 30 diffe-
rent genera, including Aeromonas, Acinetobacter, Acetobac-
ter, Achromobacter, Alcaligenes, Azospirillum, Azotobacter,
P-SOLUBILIZING AND -MOBILIZING MICROBES 45

Fig. 1 A systemic representation for the isolation of P-solubilizing microbes from diverse habitats and characterization of their plant growth-promoting
attributes, mechanisms of P solubilization, and possible biotechnological applications for agricultural sustainability. PEG = polyethylene glycol; ACC =
aminocyclopropane-1-carboxylic acid; PGP = plant-growth promotion.

Bradyrhizobium, Brevundimonas, Burkholderia, Cronobac-
ter, Cupriavidus, Delftia, Dyella, Ewingella, Herbaspiril-
lum, Inquilinus, Methylobacterium, Ochrobactrum, Pantoea,
Pseudomonas, Rahnella, Raoultella, Rhizobium, Rhodobac-
ter, Serratia, Sphingomonas, Stenotrophomonas, Vibrio, and
Xanthomonas. Firmicutes consist of 43 species belonging
to seven genera: 24 belong to Bacillus; 8 to Paenibacil-
lus; 6 to Staphylococcus; 2 to Planococcus; and 1 each to
Brevibacillus, Exiguobacterium, and Oceanobacillus. Ac-
tinobacteria consist of 28 species which belong to 10 genera;
the most dominant genera is Streptomyces (12 species), fo-
llowed by Arthrobacter, Brevibacterium, Microbacterium,
Rhodococcus, Agromyces, Clavibacter, Corynebacterium,
Micrococcus, and Nocardiopsis. Another important phy-
lum of P solubilizers is Euryarchaeota, comprising 18
species of archaea belonging to 10 genera, i.e., Haloar-
cula, Halobacterium, Halococcus, Haloferax, Halolamina,
Halostagnicola, Haloterrigena, Natrialba, Natrinema, and
46 D. KOUR et al.

Fig. 2 Abundance of P-solubilizing microbes belonging to diverse phyla (a) and diversity and distribution of different predominant genera with P-solubilization
attributes implicated in the P cycle.
P-SOLUBILIZING AND -MOBILIZING MICROBES
Natronoarchaeum. The lowest diversity of P-solubilizing
bacteria is found in the phylum Bacteriodetes, consisting
of five different species belonging to four genera: Chry-
seobacterium, Flavobacterium, Flexibacter, and Sphingoba-
cterium. Among P-solubilizing fungi, Ascomycota is the most
dominant phylum with 16 species belonging to 7 genera,
i.e., Aspergillus, Curvularia, Eupenicillium, Paecilomyces,
Penicillium, Sarocladium, and Trichoderma, followed by
the phylum Basidiomycota with 11 species belonging to 8
genera, i.e., Crytococcus, Pseudozyma, Rhodosporodium,
Rhodotorula, Sporidiobolus, Symmetrospora, Trichosporon,
and Ustilago. Mucoromycota include only three species
belonging to two genera, i.e., Absidia and Mucor (Figs. 3–6).
Phosphorus-solubilizing microbes play an important role
in the mitigation of different abiotic stresses (Yadav A et
al., 2015; Verma et al., 2016, 2019; Biswas et al., 2018). A
review of literature shows that P-solubilizing microbes from
extreme habitats, such as high/low-temperature, drought,
salinity, heavy metal-contaminated, and acidic/alkaline en-
vironments, exhibit P-solubilizing and -mobilizing activities
(Table SI). The highest diversity of P solubilizers is observed
in high temperature environments, with 37 species belonging
to 17 genera, i.e., Achromobacter, Alcaligenes, Aneurini-
bacillus, Aspergillus, Bacillus, Chaetomium, Delftia, Fusa-
rium, Methylobacterium, Mucor, Penicillium, Pseudomonas,
Rhodobacter, Salmonella, Streptococcus, Streptomyces, and
Trichoderma, followed by drought- and salinity-affected a-
reas, each with 24 species. Drought-tolerant P solubilizers
belong to 10 diverse genera: Alcaligenes, Aneurinibacillus,
Aspergillus, Bacillus, Fusa-rium, Paenibacillus, Penicil-
lium, Pseudomonas, Talaromyces, and Terribacillus. The
P-solubilizing microbes from saline environments belong
to 11 different genera: Acinetobacter, Aspergillus, Bacillus,
Chaetomium, Delftia, Enterobacter, Penicillium, Pichia,
Pseudomonas, Talaromyces, and Terribacillus. Seventeen
species of P-solubilizing microbes have been observed from
low-temperature conditions; they belong to eight genera:
Acinetobacter, Aspergillus, Bacillus, Exiguobacterium, Pae-
cilomyces, Pantoea, Pseudomonas, and Trichoderma. Six-
teen species have been obtained from acidic and alkaline
soils; they belong to nine genera: Achromobacter, Acineto-
bacter, Aspergillus, Bacillus, Exiguobacterium, Methylobac-
terium, Pichia, Pseudomonas, and Trichoderma. Fifteen
species belonging to eight genera, i.e., Azotobacter, Bre-
vundimonas, Bacillus, Enterobacter, Pseudomonas, Fusa-
rium, Methylobacterium, and Mucor, have been obtained
from heavy metal-contaminated soils. The genera Bacil-
lus and Pseudomonas have been obtained from all stress
environments (Fig. 7, Table SI).
Phosphorus solubilizers have been reported to be isolated
from plants including cereals (Verma et al., 2015; Kour et
al., 2019a; Yadav, 2019), oil crops (Shahid et al., 2015),
47
medicinal plants (Rai et al., 2018), fruit crops (Mehta et al.,
2015), and spice crops (Mishra et al., 2015; Panchami and
Karthikeyan, 2017). Among them, Acinetobacter, Azotobac-
ter, Bacillus, Enterobacter, Paenibacillus, Pseudomonas,
and Serratia are common to all crops (Table SI), whereas
Chaetomium and Microbacterium, are only from barley,
Ochrobactrum and Agromyces from bitter gourd, Micrococ-
cus and Nocardiopsis from ginger, Brevibacterium, Lysobac-
ter, and Methylobacterium from Jatropha curcas, Candida,
Clavispora, Eupenicillium, Ewingella, Meyerozyma, Rah-
nella, Rhizomucor, and Sarocladium from maize, Rhizo-
bium and Klebsiella from pea, Aeromonas, Alcaligenes, and
Brevibacterium from rice, Sinorhizobium and Acremonium
from soybean, Cupriavidus, Chlorella, Flexibacter, Labrys,
and Microbispora from sugarcane, Cronobacter, Kocuria,
and Mucor from tomato, Rhodococcus, Brevundimonas,
and Corynebacterium from walnut, and Exiguobacterium,
Planococcus, and Planomicrobium from wheat (Fig. 8).
Phosphorus-solubilizing microbes can be endophytes, epi-
phytes, and inhabitants of both rhizospheric and bulk soils
(Suman et al., 2016; Verma et al., 2017; Yadav et al., 2018;
Kour et al., 2019c). Some of the isolates are niche specific,
while others are present in more than one niche. Seven-
teen percent of them are only endophytic, 10.6% epiphytic,
7% rhizospheric soil, and 3% from bulk soil. Furthermore,
1.1% are endophytic and from bulk soil, 2% endophytic
and rhizospheric, 4.3% epiphytic and rhizospheric, 5.3%
epiphytic and from bulk soil, and 12.8% both rhizospheric
and from bulk soil. Sixteen percent are present in all four
niches mentioned above (Fig. 9).
A huge diversity of bacteria isolated from alpine and
sub-alpine regions are both tolerant to low temperature
and can solubilize P. These include Achromobacter sp.,
Acinetobacter rhizosphaerae, Bacillus megaterium, Bacil-
lus subtilis, Burkholderia vietnamiensis, Exiguobacterium
acetylicum, Mycobacterium phlei, Mycoplana bullata, Pan-
toea agglomerans, Pantoea dispersa, Pseudomonas corru-
gata, Pseudomonas fluorescens, Pseudomonas fragi, Pseu-
domonas lurida, Pseudomonas putida, Rahnella sp., Serratia
marcescens, and Tetrathiobacter sp. Among them, strains of
E. acetylicum are emerging as potential candidates for effi-
cient bioinoculants in mountainous regions (Table SI). These
strains have been also isolated from extreme environments,
e.g., Siberian permafrost, a glacial ice core sample in Green-
land, and hot springs (Vishnivetskaya et al., 2009). Vazquez
et al. (2000) reported nine strains of phosphate-solubilizing
bacteria from the arid mangrove ecosystem in Mexico, inclu-
ding those isolated from the roots of Avicennia germinans
(black mangrove), Bacillus amyloliquefaciens, Bacillus at-
rophaeus, Enterobacter aerogenes, Enterobacter asburiae,
Enterobacter taylorae, Kluyvera cryocrescens, Paenibacillus
macerans, Vibrio proteolyticus, and Xanthobacter agilis, and
48 D. KOUR et al.

Fig. 3 Phylogenetic tree showing the relationships among different phyla of P-solubilizing microbes isolated from different hosts worldwide (a) and that with
species of the phylum Actinobacteria listed (b).

those isolated from the roots of Languncularia racemosa
(white mangrove), Bacillus licheniformis, Pseudomonas lute-
ola, and Pseudomonas stutzeri. The halophilic P-solubilizing
bacteria Kushneria sinocamis has been also observed in
sediments of the Daqiao Saltern and could be used as an
inoculant in salt-affected agricultural soils (Zhu et al., 2011).
Widawati and Suliasih (2001) reported B. megaterium
and Pseudomonas sp. as dominant P solubilizers from the
rhizosphere of different plants in Gunung Halimun Na-
tional Park, Indonesia, whereas Chen et al. (2006) showed
P-SOLUBILIZING AND -MOBILIZING MICROBES 49

Fig. 4 Phylogenetic tree showing the relationships among different phyla of P-solubilizing microbes isolated from different hosts worldwide with species of
the phylum Firmicutes listed.

tricalcium phosphate (TCP) solubilizing Arthrobacter, Bacil-
lus, Chryseobacterium, Delftia, Gordonia, Phyllobacterium,
Rhodococcus, and Serratia in sub-tropical soils and re-
ported four strains, Arthrobacter ureafaciens, Delftia sp.,
Phyllobacterium myrsinacearum, and Rhodococcus erythro-
polis, for the first time as P solubilizers. Jiang et al. (2008)
reported a heavy metal- and antibiotic-resistant bacterial
strain, Burkholderia sp. J62, from heavy metal-contaminated
soils possessing the capability to solubilize inorganic P,
producing siderophores, indole acetic acid (IAA), and 1-
50 D. KOUR et al.

Fig. 5 Phylogenetic tree showing the relationships among different phyla of P-solubilizing microbes isolated from different hosts worldwide with species of
the phyla Bacteroidetes and Proteobacteria listed.
P-SOLUBILIZING AND -MOBILIZING MICROBES 51

Fig. 6 Phylogenetic tree showing the relationships among different phyla of P-solubilizing microbes isolated from different hosts worldwide with species of
the phyla Euryarchaeota, Basidiomycota, Mucoromycota, and Ascomycota listed.

aminocyclopropane-1-carboxylic acid (ACC) deaminase, and
increasing the biomass of maize and tomato plants. Naik et al.
(2008b) reported Pseudomonas aeruginosa, P. fluorescens,
Pseudomonas fulva, Pseudomonas mosselii, Pseudomonas
monteilii, Pseudomonas plecoglossicida, Pseudomonas al-
caligenes and Pseudomonas pseudoalcaligenes from the
rhizospheric soil of banana to be P solubilizers based on
genotypic, phenotypic, and 16S rRNA gene phylogenetic
analyses. In the study of Chang and Yang (2009), thermo-
tolerant P-solubilizing bacteria, actinomycetes, and fungi
were isolated from compost and biofertilizers, including
Aspergillus fumigatus, Bacillus coagulans, B. licheniformis,
52 D. KOUR et al.

Fig. 7 Diversity and distribution of different niche-specific P-solubilizing microbes isolated from diverse extreme habitats.
P-SOLUBILIZING AND -MOBILIZING MICROBES
Fig. 8 Niche-specific P-solubilization microbes isolated from host plants.
Fig. 9 Venn diagram representing the biodiversity (number and percen-
tage) of common and niche-specific P-solubilizing microbes from plant
microbiomes and soil ecosystems.
Bacillus smithii, Brevibacillus borstelensis, Streptococcus
thermophilus, and Streptomyces thermonitrificans. Kundu
et al. (2009) reported Aeromonas, Enterobacter, Klebsiella,
and Pseudomonas as predominant P-solubilizing genera from
the rhizosphere of chickpea, mustard, and wheat grown in
different areas of Haryana, India.
Symbiotic N-fixing bacteria also have shown P-solu-
bilizing activity (Zaidi et al., 2009). Liu et al. (2011) isolated
P-solubilizing bacterium P. fluorescens and P-mineralizing
bacteria Bacillus cereus and B. subtilis from the rhizosphere
of poplar from different regions of China. Ndung’u-Magiroi
et al. (2012) studied the occurrence of P-solubilizing bac-
teria in soils of varied chemical properties in Kenya and
identified several species including Arthrobacter, Bacillus,
Burkholderia, Curtobacterium, Microbacterium, Micrococ-
53
cus, Paenibacillus, and Pseudomonas, with Arthrobacter
sp., B. megaterium, and Paenibacillus sp. being the most
abundant. The study of Ambrosini et al. (2012) has found
that Burkholderia strains associated with sunflower plants
solubilize TCP. Yang et al. (2012) isolated 1 328 bacteria
from P-rich soil in the drainage area of Dianchi Lake, China,
with 377 isolates exhibiting TCP solubilization of 33.48–
69.63 mg L−1 and 123 isolates showing TCP solubilization
of more than 54.00 mg L−1 . Their analysis of restriction
fragment length polymorphism (RFLP) revealed 32 unique
RFLP patterns; on the basis of these patterns, they selec-
ted 62 representative isolates for 16S rRNA sequencing.
Furthermore, on the basis of phylogenetic analysis, they
found 123 P-solubilizing bacteria belonging to three phyla,
Proteobacteria, Firmicutes, and Actinobacteria, 107 isolates
represented by 26 RFLP patterns being associated with the
genera Acinetobacter, Burkholderia, Cedecea, Enterobacter,
Klebsiella, Leclercia, Pseudomonas, Pantoea, Raoultella,
and Serratia, with Firmicutes being the subdominant group,
13 isolates being associated with the genera Bacillus and Bre-
vibacterium, and the remaining three isolates being identified
as a species of the genus Arthrobacter.
Inui-Kishi et al. (2012) identified Arthrobacter sp.,
Burkholderia gladioli, Burkholderia sp., Chlorella protothe-
coides, Enterobacter homaechei, Enterobacter sp., Flexibac-
ter sancti, and Labrys portucalensis as P solubilizers from
the rhizosphere of sugarcane. Nabti et al. (2013) isolated
halophilic B. licheniformis and Bacillus sp. from the rhi-
zosphere of potato and reported their P-solubilizing ability
and other plant growth-promoting attributes. de Souza et al.
(2013) observed that Burkholderia, Cedecea, Cronobacter,
Enterobacter, Pantoea, and Pseudomonas associated with
54
rice plants could solubilize TCP. KumarV et al. (2013) iso-
lated phytase-producing Achromobacter sp., Tetrathiobacter
sp., and Bacillus sp. from soil samples collected from the
Uttarakhand region of India, with the capacity to mineralize
and solubilize P. Harinathan et al. (2014) identified Ente-
robacter cancerogenus as an efficient P solubilizer from the
rhizospheric soil of Morinda tinctoria and Prosopis juliflora.
Bumunang and Babalola (2014) isolated rhizobacteria
from field-grown genetically modified and non-genetically
modified maize in South Africa after 30 d of sowing and
post-harvest, screened the isolates for various plant growth-
promoting attributes, including P solubilization, ammonia,
IAA, and hydrogen cyanide (HCN) production, and cata-
lase and antifungal activities, and reported 90.6% of the
isolates as P solubilizers, including Burkholderia cepa-
cia, P. luteola, P. putida, Sphingomonas paucimobilis, and
Stenotrophomonas maltophilia from genetically modified
maize and Achromobacter xylosoxidans, Bacillus safensis,
B. cepacia, Ewingella americana, P. putida, P. stutzeri, S.
maltophilia, and S. paucimobilis from non-genetically mo-
dified maize. Nandini et al. (2014) isolated P-solubilizing
Alcaligenes faecalis from the rhizospheric soil of upland
rice. Shahid et al. (2015) identified the P-solubilizing bac-
teria A. faecalis and Bacillus sp. from sunflower plants and
soils collected from various locations in Pakistan on the
basis of 16S rRNA. In the study of Mishra et al. (2015),
P-solubilizing bacteria were isolated from rhizospheric soils
of fennel (Foeniculum vulgare Mill.) from Rajasthan, India,
with Bacillus sp. and Pseudomonas sp. being the dominant
genera. Aarab et al. (2015a) found 136 TCP solubilizers, out
of 305 rhizobacteria isolated from the rhizospheric soil of
rice in Northern Morocco, with Aeromonas, Pseudomonas,
and Enterobacter being the dominant genera as revealed by
analysis of 16S rDNA. Aarab et al. (2015b) also isolated
283 bacteria belonging to the genus Pseudomonas from
the rhizospheric soil of rice, with 67.14% of the isolates
possessing the capability to solubilize P.
Yadav A et al. (2015) isolated P-solubilizing haloar-
chaea from sediment, water, and rhizospheric soil in Rann
of Kutch, Gujrat, and identified them as Haloarcula sp.,
Halobacterium sp., Halococcus sp., Haloferax sp., Halo-
lamina sp., Halosarcina sp., Halostagnicola sp., Haloter-
rigena sp., Natrialba sp., Natrinema sp., and Natronoar-
chaeum sp. Midekssa et al. (2015) isolated 41 P-solubilizing
rhizobacteria from lentil, including genera Acinetobac-
ter, Agrobacterium, Bacillus, Burkholderia, Chryseomonas,
Enterobacter, Pseudomonas, Ralstonia, and Sphingomonas,
and evaluated their effects on the growth of lentil under
greenhouse conditions. Chauhan et al. (2017) isolated the P-
solubilizing strain Aneurinibacillus aneurinilyticus CKMV1
from the rhizosphere of Valeriana jatamansi and found P
solubilization of 260 mg L−1 . Bashir et al. (2018) isolated
D. KOUR et al.
P-solubilizing rhizobacteria from apple and characterized
them on a morphological and biochemical basis.
A few studies have been carried out on yeasts for their
capability to solubilize P including Yarrowia lipolytica,
Schizosaccharomyces pombe, and Pichia fermentans (Vas-
silev et al., 2001). Among the filamentous fungi, the domi-
nant P-solubilizing genera include Aspergillus and Penicil-
lium (Fenice et al., 2000; Khan and Khan, 2002). Some
strains of Trichoderma (Altomare et al., 1999) and Rhizoc-
tonia solani (Jacobs et al., 2002) have also been reported
to be P solubilizers. Duponnois et al. (2006) reported the
nematophagous fungus Arthrobotrys oligospora to be a
P solubilizer both under in vitro and in vivo conditions.
Pandey et al. (2008) identified the P solubilizers Penicillium
citrinum, Penicillium janthinellum, Penicillium oxalicum,
Penicillium pinetorum, Penicillium pinophilum, Penicillium
purpurogenum, and Penicillium raistrickii isolated from soils
of Indian Himalayan region. Yasser et al. (2014) isolated
Trichoderma harzianum, Trichoderma koningii, Penicillium
variable, P. purpurogenum, Penicillium funiculosum, Penicil-
lium expansum, Aspergillus niger, and Aspergillus japonicas
from Egyptian soils to solubilize inorganic phosphate. Pot-
shangbam et al. (2017) isolated endophytic P-solubilizing
fungi, including Acremonium sp., Aspergillus ustus, Fusa-
rium oxysporum, Penicillium simplicissimum, Rhizomucor
sp., Sarocladium strictum, and Trichoderma koningiopsis,
from maize and rice plants.
The ability of actinomycetes to solubilize P has attracted
great attention. Hamdali et al. (2008) reported that 20%
of actinomycetes solubilize P, and the dominant genera are
Streptomyces and Micromonospora. Jog et al. (2014) iso-
lated P-solubilizing Streptomyces cellulosae, Streptomyces
cheonanensis, Streptomyces lomondensis, and Streptomyces
werraensis from the rhizosphere of wheat. Gangwar et al.
(2015) isolated endophytic Streptomyces cinereus and Strep-
tomyces griseofuscus, P solubilizers, from Indian gooseberry
plants.
MECHANISMS OF P-SOLUBILIZING MICROBES
The important processes affecting P concentrations
are dissolution-precipitation and sorption-desorption. The
main mechanisms employed for P solubilization by soil
microorganisms consist of the release of complexing or
mineral-dissolving compounds, such as organic acid anions,
siderophores, protons, hydroxyl ions, and CO2 , and the
liberation of various extracellular enzymes (Table I).
Mineralization of organic phosphate
High-molecular-weight organic forms of P cannot be
taken up by the plants directly and are usually trans-
formed into inorganic forms after being mineralized. Organic
P-SOLUBILIZING AND -MOBILIZING MICROBES 55

TABLE I
Organic acids produced during the solubilization process by P-solubilizing microbes
Microbe Organic acid(s) Reference
Enterobacter intermedium 2-Ketogluconic acid Hwangbo et al. (2003)
Citrobacter sp. DHRSS Acetic acid, gluconic acid Patel et al. (2008)
Talaromyces helicus L7b Acetic acid, citric acid, fumaric acid, lactic acid, malic acid, butyric Scervino et al. (2010)
acid
Halolamina sp. IARI-CDK2 Citric acid, gluconic acid Yadav A et al. (2015)
Penicillium rugulosum Citric acid, gluconic acid Reyes et al. (2001)
Haloterrigena sp. IARI-SNAB3 Citric acid, formic acid, gluconic acid, propionic acid, succinic Yadav A et al. (2015)
acid, fumaric acid, tartaric acid
Haloterrigena thermotolerans IARI-SNAB1 Citric acid, formic acid, gluconic acid, propionic acid, succinic acid Yadav A et al. (2015)
Halosarcina sp. IARI-WRAB3 Citric acid, gluconic acid, succinic acid Yadav A et al. (2015)
Serratia marcescens CC-BC14 Citric acid, gluconic acid, succinic acid, lactic acid, unknown acid Chen et al. (2006)
Arthrobacter sp. CC-BC03 Citric acid, lactic acid Chen et al. (2006)
Bacillus megaterium CC-BC10 Citric acid, lactic acid, unknown acid Chen et al. (2006)
Halococcus sp. IARI-SNAB2 Fumaric acid, citric acid, gluconic acid Yadav A et al. (2015)
Talaromyces flavus S73 Fumaric acid, citric acid, gluconic acid, succinic acid, lactic acid, Scervino et al. (2010)
valeric acid
Penicillium purpurogenum POP Fumaric acid, citric acid, gluconic acid, succinic acid, malic acid, Scervino et al. (2010)
valeric acid
Penicillium janthinellum PJ Fumaric acid, gluconic acid, succinic acid, lactic acid, citric acid, Scervino et al. (2010)
glucuronic acid
Azospirillum brasilense 8-I Gluconic acid Rodríguez et al. (2004)
Azospirillum lipoferum JA4 Gluconic acid Rodríguez et al. (2004)
Burkholderia cepacia DA23 Gluconic acid Song et al. (2008)
Burkholderia sp. Gluconic acid Pérez et al. (2007)
Pantoea sp. Gluconic acid Pérez et al. (2007)
Pseudomonas aeruginosa Gluconic acid Patel et al. (2011)
Ralstonia sp. Gluconic acid Pérez et al. (2007)
Serratia sp. Gluconic acid Pérez et al. (2007)
Streptomyces cellulosae mhcr0816 Malic acid Jog et al. (2014)
Streptomyces tricolor mhce0811 Gluconic acid Jog et al. (2014)
Bacillus circulans CB7 Gluconic acid, citric acid Mehta et al. (2015)
Halobacterium sp. IARI-SNS3 Gluconic acid, citric acid, formic acid, propionic acid Yadav A et al. (2015)
Haloferax alexandrinus IARI-MAAB1 Gluconic acid, citric acid, formic acid, propionic acid Yadav A et al. (2015)
Haloferax sp. IARI-MAAB2 Gluconic acid, citric acid, formic acid, propionic acid, succinic acid Yadav A et al. (2015)
Halococcus hamelinensis IARI-SNS2 Gluconic acid, citric acid, formic acid, succinic acid, tartaric acid Yadav A et al. (2015)
Haloarcula argentinensis IARI-SOAB1 Gluconic acid, citric acid, fumaric acid, propionic acid, Yadav A et al. (2015)
Haloterrigena thermotolerans IARI-SGAB1 Gluconic acid, citric acid, propionic acid, fumaric acid, Yadav A et al. (2015)
Natrialba sp. IARI-SGAB2 Gluconic acid, citric acid, propionic acid, succinic acid, fumaric Yadav A et al. (2015)
acid, tartaric acid
Haloferax volcanii IARI-SSAB5 Gluconic acid, citric acid, succinic acid, fumaric acid Yadav A et al. (2015)
Halolamina pelagica IARI-CSK1 Gluconic acid, citric acid, succinic acid, fumaric acid, tartaric acid Yadav A et al. (2015)
Natronoarchaeum mannanilyticum IARI-SSAB3 Gluconic acid, fumaric acid Yadav A et al. (2015)
Natrinema sp. IARI- WRAB2 Gluconic acid, fumaric acid, succinic acid Yadav A et al. (2015)
Haloferax larsenii IARI-CFAB1 Gluconic acid, propionic acid Yadav A et al. (2015)
Halobacterium sp. IARI-SSAB1 Gluconic acid, propionic acid, tartaric acid Yadav A et al. (2015)
Haloferax larsenii IARI-WAB1 Gluconic acid, tartaric acid Yadav A et al. (2015)
Rhodococcus erythropolis Gluconic acid, unknown acid Chen et al. (2006)
Bacillus megaterium CC-BC26 Lactic acid, propionic acid Chen et al. (2006)
Pichia farinose FL7 Oxalic acid, malic acid, lactic acid, acetic acid, citric acid, succinic Zhu et al. (2012)
acid
Bacillus megaterium CC-BC29 Propionic acid Chen et al. (2006)

transformation and mineralization are catalyzed by different
soil enzymes. The phosphatases in soil hydrolyze soil organic
P into its inorganic forms, such as HPO− −
4 and H2 PO4 , before
it can be utilized and taken up from the soil solution by the
plant roots. Phosphatases are capable of hydrolyzing both
phosphate ester and anhydride bonds, including acid and al-
kaline phosphatases, diadenosine tetraphosphatases, exonu-
cleases, phosphoprotein phosphatases, phosphodiestrases,
50 -nucleotidases, phytases, and acid phosphomonoesterases
(Nannipieri et al., 2011). The mineralization of organic P
by microbes is strongly influenced by the environmental
parameters; in fact, mineralization is mostly favored in envi-
ronments with moderate alkalinity. There are non-specific
acid phosphatases, which can cause dephosphorylation of
the phosphoester or phosphoanhydride bonds present in
the organic matter. Many soil microbial species, including
Aspergillus, Bacillus, Mucor, Penicillium, Rhizopus, Pseu-
domonas, and mycorrhizal hyphae, are known to produce
phosphatases (Behera et al., 2014; Shrivastava et al., 2018).
56
Acid phosphatases dominate in acidic soils, whereas
alkaline phosphatases dominate in neutral and alkaline soils
(Yu et al., 2006). The release of the orthophosphate ions
HPO− −
4 and H2 PO4 from organic forms of P in soil is me-
diated by both plants and phosphatases, with an indication
that the phosphatases produced by the microbes are more
efficient (Tarafdar et al., 2001). There are a number of acid
phosphatase genes isolated and characterized from Gram-
negative bacteria. One example is the gene acpA, isolated
from Francisella tularensis, expressing an acid phosphatase
with optimum activity at pH 6 and a wide range of substrate
specificity (Reilly et al., 1996). A gene from B. cepacia facili-
tating phosphatase activity has also been isolated (Rodríguez
et al., 2000). Additionally, two non-specific periplasmic acid
phosphatase genes, napD and napE, from Sinorhizobium
meliloti have also been cloned (Deng et al., 1998, 2001).
Acid phosphatases have also been reported to be from the
fungus Aspergillus tubengensis (Achal et al., 2007).
Most phytases are high-molecular-weight acid phos-
phatases catalyzing the release of P from phytate, which is
an ester of inositol and the major stored P form in seeds and
pollens (Rodríguez et al., 2006). The capability of the plants
to directly obtain P from phytate is very limited. The study of
Richardson et al. (2001b) demonstrates the enhancement in
growth and P nutrition of Arabidopsis genetically modified
with the gene phyA from A. niger with supply of phytate.
It has also been reported that the enhanced utilization of
inositol phosphate by plants occurs in the presence of soil
microorganisms (Richardson et al., 2001a). The phytase
genes appA and appA2 from Escherichia coli were also
isolated and characterized (Golovan et al., 1999; Rodrıìguez
et al., 1999). Neutral phytase genes from B. subtilis and
B. licheniformis have also been cloned (Tye et al., 2002).
The gene phyA from the plant growth-promoting bacte-
ria B. amyloliquefaciens (Idriss et al., 2002) possesses the
highest extracellular phytase activity; additionally, diluted
culture filtrates of these strains stimulate the growth of maize
seedlings when grown under limited P conditions in the
presence of phytate. Kumar V et al. (2013) reported growth
promotion of Brassica juncea and increase in its P content
with phytase-producing bacteria such as Tetrathiobacter sp.
and Bacillus sp.
In the study of Yadav and Tarafdar (2003), Aspergillus,
Emmericella, and Penicillium isolated from arid and semi-
arid regions of India showed phytin- and glycerophosphate-
hydrolyzing activity. In the study of Zhao et al. (2017),
Trichoderma asperellum Q1 isolated from the rhizosphere
of cucumber produced acid and alkaline phosphatases and
showed high P-solubilizing activity and purified acid phos-
phatases contributed to the growth of Arabidopsis thaliana.
This study is the first report on purification of acid phos-
phatase from T. asperellum and its role in stimulating the
growth of plants under salt stress.
D. KOUR et al.
All of these reports mentioned above directly confirm
that phytase activity plays an important role in stimulating
plant growth on limited-P soil, thus supporting the potential
use of phytase genes for the improvement or transfer of
P-solubilizing traits to plant growth-promoting bacterial
strains used as agricultural bioinoculants. Furthermore, there
are a number of bacteria that have been isolated from the
rhizospheric soils of different plants, such as Avena sativa,
Lolium perenne, Lupinus luteus, and Trifolium repens; they
have been reported to be helpful in both the production of
organic acids for the solubilization of inorganic P and the
production of phytase to mineralize phytate (Jorquera et al.,
2011).
Mineralization of inorganic P
A broad range of mechanisms exist in nature for P solu-
bilization by bacteria and fungi. The major mechanism for
the solubilization of inorganic P is the production of organic
acids by microbes, which lowers the pH of the rhizospheric
soil or chelates the cations that are responsible for P pre-
cipitation. They may compete with P for sorption sites on
the soil or may form the soluble complexes with metal ions
associated with insoluble P compounds, such as phosphates
of aluminum, calcium, and iron (Shrivastava et al., 2018).
Thus, the produced organic acids directly dissolve the mine-
ral P (Omar, 1997). Organic acids commonly produced by P
solubilizers include aspartic acid, citric acid, gluconic acid,
lactic acid, oxalic acid, and tartaric acid (Venkateswarlu et
al., 1984; Kim et al., 1997; Di Simine et al., 1998; Bar-Yosef
et al., 1999). Rodrıìguez et al. (2004) studied the forma-
tion of acid and phosphate solubilization by Azospirillum
brasilense and Azospirillum lipoferum. Both species were
found to produce gluconic acid when grown in a sparingly
soluble calcium phosphate medium, reducing the pH of
the medium and releasing soluble P. Vilcram et al. (2007)
tested P-solubilizing bacteria for the production of organic
acids, such as fumaric, citric, gluconic, maleic, tartaric,
and succinic acid, as well as other unidentified acids and
found production of all the six organic acids by the strain
PSBV-9 and only five organic acids by PSBV-10, PSBV-25,
and PSBV-16. Hariprasad and Niranjana (2009) reported the
increased growth in Lycopersicon esculentum because of the
presence of Enterobacter sp., which produced gluconic acid,
solubilizing calcium phosphate. However, acidification alone
is not the universal mechanism of solubilization; there are
some reports that show microbial P solubilization without
the production of organic acids. For example, Altomare et
al. (1999) showed that T. harzianum solubilizes P without
the detection of organic acids. Moreover, Nitrosomonas and
Thiobacillus produce only nitric and sulfuric acids, which
may solubilize P (Teotia et al., 2016; Bahadur et al., 2017).
P-SOLUBILIZING AND -MOBILIZING MICROBES
Role of exopolysaccharides in P solubilization
Exopolysaccharides are carbohydrates polymers that are
excreted by some bacteria and fungi outside their cell walls.
They may either be homopolysaccharides or heteropolysac-
charides and may have numerous different organic and ino-
rganic substituents. Exopolysaccharides can form complexes
with metals in soil. Yi et al. (2008) reported that P solubilizers
such as Arthrobacter sp., Azotobacter sp., and Enterobacter
sp. produce a significant amount of exopolysaccharides. Tak-
tek et al. (2017) showed that exopolysaccharide-producing
rhizobacteria solubilize igneous phosphate rock by secreting
viable biofilm cells and organic acids.
Mobilization of P
Arbuscular mycorrhizal (AM) fungi. Arbuscular
mycorrhizal fungi are greatly beneficial to the majority of
plant cultivars and play an important role in the conservation
of the environment by acting as biofertilizers, biocontrol
agents, and bioprotectors (Azcón-Aguilar et al., 2002; Thila-
gar and Bagyaraj, 2015). These soil fungi are known to aid in
the uptake of diffusion-limited nutrients (particularly P) and
increase crop production (Joner, 2000; Gaur and Adholeya,
2002). According to Jones et al. (1998), the efficiency of
mycorrhizal plants in the uptake of P is about 3.1–4.7 times
higher than that of nonmycorrhizal plants. The AM fungi in
agriculture can reduce the use of chemical fertilizers and help
in sustaining plant productivity and retaining soil quality
(Surendran and Vani, 2013). Hence, one of the best alterna-
tives to increase the P supply to plants is using AM fungi as
inoculants (Osorio and Habte, 2001). Thilagar and Bagyaraj
(2015) inoculated chilly plants with diverse species of AM
fungi, such as Acaulospora laevis, Gigaspora margarita,
Glomus bagyarajii, Glomus etunicatum, Glomus fascicu-
latum, Glomus intraradices, Glomus leptotichum, Glomus
macrocarpum, Glomus monosporum, Glomus mosseae, and
Scutellospora calospora and found that G. mosseae is the best
in terms of bio-volume index, fruit yield, P uptake, and plant
biomass. Kumar A et al. (2016a) concluded that AM fungal
inoculation can potentially increase system productivity and
profitability, decreasing the inorganic P requirement by about
25% in an okra-pea production system on Himalayan acid
Alfisol. Furthermore, it has been well demonstrated that
the combined inoculation of arbuscular mycorrhizas and P-
solubilizing microbes results in an improved uptake of both
native P from soil and P from phosphatic rock (Cabello et al.,
2005). Ratti et al. (2001) inoculated Cymbopogon martinii
with the AM fungus Glomus aggregatum, the P-solubilizing
rhizobacterium Bacillus polymyxa, and the N2 -fixing bac-
terium A. brasilense. They found that these rhizobacteria
behave as mycorrhiza helper bacteria and increase root colo-
nization by G. aggregatum in the presence of TCP. Dutta
57
and Neog (2017) evaluated the roles that AM fungi and
plant growth-promoting rhizobacteria play in modulating P
dynamics in the rhizosphere of turmeric.
Piriformospora indica. Piriformospora indica, a
basidiomycete fungal endophyte, has attained significant
interest as a potential growth-promoting agent (Chhabra and
Dowling, 2017). This endophyte was originally reported to be
from the roots of xerophytic woody shrubs such as P. juliflora
and Zizyphus nummularia in the Thar Desert, India (Varma
et al., 1999; Johnson et al., 2014). It is easily cultivable
and endophytically colonizes the roots of many agricultural,
floricultural, horticultural, medicinal, and agroforestry plants
(Oelmüller et al., 2009; Johnson et al., 2014). It can promote
plant growth, stimulate seed production, and possesses broad
host-range specificity (Singh et al., 2000, 2011). It has many
properties similar to AM fungi and possesses the capability
to colonize the roots of a broad range of higher plants,
including those that cannot form symbioses with AM fungi,
thus promoting nutrient uptake, disease resistance, stress tole-
rance, and growth of their hosts (Hosseini et al., 2017; Hussin
et al., 2017; Xu et al., 2017; Wu et al., 2018). It could act as
a model system to study the mechanisms responsible for host
growth or fitness; it is capable of mobilizing unavailable P for
plant uptake by producing extracellular phosphatases (Singh
et al., 2000; Thilagar and Bagyaraj, 2015). This endophyte
can solubilize P from inorganic sources by decreasing the
pH of the medium (Ngwene et al., 2016). The high-affinity
phosphate transporter PiPT isolated from an endophyte
has been identified and functionally characterized as being
essential for the transport of P to the host plant (Yadav et
al., 2010). However, the mechanism of P transport from the
fungus to the host is not clear; it has been hypothesized that
the transfer process may occur at the plant-fungus interface
and requires two transporters, one enabling the P efflux from
the fungus and the other mediating the P uptake by the host
plant (Rausch and Bucher, 2002). It has been suggested that
P. indica could be used in the field as a biocontrol agent,
biofertilizer, bioregulator, or growth and yield stimulator
(Malla et al., 2004).
GENOMICS OF P-SOLUBILIZING MICROBES
Genes responsible for P solubilization
The mineral P-dissolving ability of bacteria is associated
with the production of organic acid (Rodrıguez and Fraga,
1999). The direct oxidation of glucose to gluconic acid has
been proposed by Goldstein (1994) as the main mechanism
for mineral phosphate solubilization in Gram-negative bac-
teria. The biosynthesis of gluconic acid is carried out by the
enzyme glucose dehydrogenase (GDH), which is a quinopro-
tein enzyme and requires pyrroloquinoline quinone (PQQ) as
a redox co-factor. There are two types of GDHs, GDH-A and
58 D. KOUR et al.

GDH-B. Various bacterial species, such as Acinetobacter
calcoaceticus, Acinetobacter lwoffii, E. coli, Gluconobac-
ter suboxydans, Klebsiella aerogenes, and P. aeruginosa,
can contain GDH-A, which is a membrane-bound enzyme,
whereas GDH-B, a soluble enzyme, is only reported in A.
calcoaceticus (Cleton-Jansen et al., 1988).
Various genes involved in mineral phosphate solubiliza-
tion have been isolated from different species (Table II).
Expression of genes involved in mineral phosphate solubi-
lization from Erwinia herbicola in E. coli HB101 allows
the production of gluconic acid and confers the capacity
to solubilize hydroxyapatite (Liu et al., 1992). Kim et al.
(1998) cloned genes (mps) expressing the mineral phosphate-
solubilizing trait from Rahnella aquatilis in E. coli HB101,
resulting in higher amounts of soluble phosphate and glu-
conic acid than R. aquatilis. Kim et al. (2003) included
the gene pqq from rhizobacteria Enterobacter intermedium
60-2G, expressing the capability to solubilize insoluble P
into the genome of E. coli DH5α, ultimately conferring the
capability to solubilize P from hydroxyapatite by decreasing
its pH. Sashidhar and Podile (2009) induced the GDH gene
(gcd) from E. coli into the genome of Azotobacter vinelandii
AvOP, and bacterized seeds of sorghum with transgenic
Azotobacter expressing the gene gcd, increasing the mine-
ral phosphate solubilization potential. Miller et al. (2010)
screened a transposon mutant library of P. fluorescens F113
for mutants with a reduced capacity of solubilizing TCP.
They found that mutations in the gcd and pqqE genes greatly
reduce the capability to solubilize P, whereas mutations in the
gene pqqB only moderately affect the P-solubilizing capacity.
Their study revealed that changes in the pqq biosynthetic
genes and the presence or absence of the gluconate dehy-
drogenase gene (gad) essentially affect the P-solubilizing
capability of strains of P. fluorescens.
In the study of Kumar C et al. (2013), Enterobacter
asburiae PS13, an efficient P solubilizer, was modified to
express the gluconate dehydrogenase operon (gad) of P.
putida KT2440 so that it could produce 2-ketogluconic acid,
and the modified E. asburiae PSI3 harboring the operon
gad secreted about 11.63 mmol L−1 of 2-ketogluconic and
21.65 mmol L−1 of gluconic acids and solubilized 0.84
mmol L−1 of P from rock phosphate. Wagh et al. (2014)
over-expressed the gene pqqE of E. herbicola and the pqq
gene clusters of P. fluorescens B16 and A. calcoaceticus in

TABLE II
Genes and gene expression in P solubilization attributes from P-solubilizing microbes
Microbe
Deinococcus radiodurans
Rahnella aquatilis
Serratia marcescens
Enterobacter intermedium
Acinetobacter calcoaceticus
Pseudomonas fluorescens
Erwinia herbicola
Pseudomonas cepacia
Zymomonas mobilis
Saccharomyces cerevisiae
Vitreoscilla hemoglobin
Penicillium oxalicum
Bacillus licheniformis
Synechococcus elongatus
Escherichia coli
Aeromonas hydrophila
Gene(s) Expression microbe P solubilization attribute(s) Reference
pqq Escherichia coli Mineral phosphate solubilization phenotype Khairnar et al. (2003)
mps E. coli Mineral phosphate solubilization phenotype, Kim et al. (1998)
gluconic acid production
pqq E. coli Mineral phosphate solubilization phenotype Kim et al. (2006)
gdh, pqqABCDE E. coli Enhanced mineral phosphate solubilization Farhat et al. (2013)
pqq E. coli Mineral phosphate solubilization phenotype, Kim et al. (2003)
gluconic acid production
pqq Herbaspirillum Pyrroloquinoline quinone (PQQ) secretion, Wagh et al. (2014)
seropedicae gluconic acid production
pqq H. seropedicae PQQ secretion, gluconic acid production Wagh et al. (2014)
pqq Burkholderia Enhanced mineral phosphate solubilization Rodríguez et al. (2000)
cepacia
pqq Pseudomonas sp. Enhanced mineral phosphate solubilization Rodríguez et al. (2000)
pqq E. coli Mineral phosphate solubilization phenotype, Liu et al. (1992)
gluconic acid production
gabY E. coli Mineral phosphate solubilization phenotype, Babu-Khan et al. (1995)
gluconic acid production
invB Enterobacter Mineral phosphate solubilization, gluconic Kumar C et al. (2016)
asburiae acid production
suc2 E. asburiae Mineral phosphate solubilization, gluconic Kumar C et al. (2016)
acid production
vgb Enterobacter Enhanced mineral phosphate solubilization Yadav et al. (2014)
hormaechei
p5cdh E. coli Increased secretion of acetic acid and Gong et al. (2014)
α-ketoglutarate, enhanced P solubilization
mMDH E. coli Enhanced organic acid secretion, improved Lü et al. (2012)
phosphate solubilization
pqq E. coli Enhanced mineral phosphate solubilization Abdel-Salam et al. (2013)
ppc Pseudomonas Enhanced phosphate solubilization Buch et al. (2010)
fluorescens
gcd Azotobacter Improved mineral phosphate solubilization Sashidhar and Podile (2009)
vinelandii
gdh E. coli Mineral phosphate solubilization, gluconic Park et al. (2008)
acid production
P-SOLUBILIZING AND -MOBILIZING MICROBES 59

the genome of Herbaspirillum seropedicae Z67 and found
that the transformants of H. seropedicae Z67 wild-type strain
pSS2 and pOK53 attain a high GDH activity and secret
about 33.46 mmol L−1 of gluconic acid and 125.47 and
168.07 µmol L−1 of P, respectively.
1.38 from Oryza sativa (Shankar et al., 2012; Megías et
al., 2018; Potshangbam et al., 2018), Serratia fonticola
AU-AP2C from Pisum sativum (Devi et al., 2013b), and
Caulobacter flavus RHGG3T from Citrullus lanatus (Yang
et al., 2019) (Table IV).

Novel P-solubilizing microbes Plant growth-promoting attributes of P-solubilizing microbes

Diverse novel species of P-solubilizing microbes has
been reported from various sources, such as rhizosphere
soils (Madhaiyan et al., 2015), medicinal plants (Suarez et
al., 2014; Nguyen et al., 2015), cereal crops (Loganathan
and Nair, 2004; Witzel et al., 2012), fresh water (Li et al.,
2017), and bulk soils (Lee et al., 2011; Toro et al., 2013;
Guo et al., 2015; Kang et al., 2019) (Table III).
Genome sequencing of P-solubilizing microbes
The genome sequences may be analyzed to obtain the
complete genetic information, obtain insight into beneficial
traits, and thus elucidate plant-microbe interactions. In the
last few decades, we have obtained information on the genome
sequences of diverse P-solubilizing microbes, such as R.
aquatilis HX2, Raoultella ornithinolytica TNT, Pantoea sp.
3.5.1, and Ochrobactrum intermedium SA148 isolated from
soil (Guo et al., 2012; Thijs et al., 2014; Suleimanova et al.,
2015; Lafi et al., 2017), P. putida MTCC5279 from Cicer
arietinum (Chaudhry et al., 2013), Pantoea sp. AS-PWVM4
and Paraburkholderia tropica P-31 from Punica granatum
(Khatri et al., 2013; Kaur et al., 2016), Arthrobacter agilis
L77 from a subglacial lake (Singh et al., 2016), Enterobacter
cloacae GS1, Bacillus altitudinis Lc5, and Pantoea ananatis
Phosphorus-solubilizing microbes can enhance plant
growth by changing the concentrations of various phyto-
hormones such as IAA (Wani et al., 2007a,b), carrying
out symbiotic or asymbiotic N fixation and soil conditio-
ning by synthesizing siderophores (Vassilev et al., 2006),
exhibiting biocontrol activity (Pandey et al., 2006), produ-
cing antibiotics and HCN (Yang et al., 2008), synthesizing
ACC deaminase (Anandham et al., 2008; Poonguzhali et
al., 2008), and reducing the toxicity of heavy metals (Khan
et al., 2009). All of these growth-promoting abilities of P-
solubilizing microbes vary under different ecological niches
(Table V). The microbes that solubilize P can simultaneously
produce IAA; a few genera of Rhizobia can both solubilize P
and secrete IAA (Pandey and Maheshwari, 2007; Badawi et
al., 2011); they act as biocontrol agents and suppress various
soil-borne phytopathogens, thereby enhancing the growth
of plants (Anbuselvi et al., 2015; Ndungu-Magiroi et al.,
2015; Kour et al., 2019b, 2020). For example, P-solubilizing
microbes can simultaneously synthesize and release vari-
ous pathogen-suppressing metabolites, such as siderophores
and lytic enzymes (Pandey et al., 2006; Rane et al., 2008).
Various P-solubilizing bacteria, such as Chromobacterium
violaceum, P. aeruginosa, and P. fluorescens, can secrete

TABLE III
Diverse novel P-solubilizing microbes reported from diverse habitats worldwide
Microbe Habitat Reference
Arachidicoccus rhizosphaerae Vu-144T Rhizosphere Madhaiyan et al. (2015)
Burkholderia metalliresistens D414T Soil Guo et al. (2015)
Citricoccus lacusdiani JXJ CY 21T Microcystis sp. Zhang et al. (2016b)
Cupriavidus yeoncheonense DCY86T Soil Singh et al. (2015)
Hartmannibacter diazotrophicus E19T Plantago winteri Suarez et al. (2014)
Microbacterium lacusdiani JXJ CY 01T Microcystis aeruginosa Zhang B H et al. (2017)
Microbacterium panaciterrae DCY56T Ginseng Nguyen et al. (2015)
Microbacterium ulmi XIL02T Ulmus nigra Rivas et al. (2004)
Modestobacter lacusdianchii JXJ CY 19T M. aeruginosa Zhang et al. (2016a)
Paenibacillus telluris PS38T Soil Lee et al. (2011)
Paenibacillus yonginensis DCY84T Soil Sukweenadhi et al. (2014)
Pseudomonas guariconensis PCAVU11T Soil Toro et al. (2013)
Pseudomonas helmanticensis OHA11T Soil Ramírez-Bahena et al. (2014)
Pseudomonas lutea OK2T Grass Peix et al. (2004)
Pseudomonas rhizosphaerae IH5T Grass Peix et al. (2003)
Rhizobium panacihumi DCY116T Soil Kang et al. (2019)
Sphingobacterium pakistanensis NCCP-246T Vigna mungo Ahmed et al. (2014)
Spirosoma lacussanchae CPCC 100624T Fresh water Li et al. (2017)
Streptomyces hundungensis MBRL 251T Soil Nimaichand et al. (2013)
Swaminathania salitolerans PA51T Rice Loganathan and Nair (2004)
Enterobacter radicincitans DSM16656T Wheat phyllosphere Witzel et al. (2012)
Caulobacter flavus RHGG3T Citrullus lanatus Yang et al. (2019)
60 D. KOUR et al.

TABLE IV
Genome sequencing data of P-solubilizing microbes isolated from diverse habitats worldwide
Microbe Host Genome DNA GC Protein-coding Total Reference
size content genes genes
Mbp %
Acinetobacter oleivorans PF1 Poplar tree 3.76 38.6 3 129 3 593 Gkorezis et al. (2015b)
Aquitalea magnusonii H3 Lemna minor 4.85 59.3 4 407 4 576 Ishizawa et al. (2017)
Arthrobacter agilis L77 Subglacial lake 3.6 69.79 3 316 3 390 Singh et al. (2016)
Arthrobacter sp. SPG23 Soil 4.7 65.7 4 088 4 276 Gkorezis et al. (2015a)
Bacillus altitudinis Lc5 Oryza sativa 3.62 41.4 3 651 3 782 Potshangbam et al. (2018)
Bacillus megaterium JX285 Camellia oleifera 5.61 37.9 5 328 5 767 Huang et al. (2019)
Bacillus methylotrophicus FKM10 Apple rhizosphere 3.9 46.5 3 678 3 889 Wang et al. (2016)
Bacillus sp. RZ2MS9 Guarana 5.29 35 5 331 5 681 Batista et al. (2016)
Bacillus sp. CPSM8 Sediment 4.39 45.9 4 521 – Maitra et al. (2014)
Burkholderia cenocepacia 869T2 Vetiver grass 7.97 67.1 7 036 7 399 Ho and Huang (2015)
Burkholderia sordidicola S170 Soil 10.26 59.6 8 782 9 107 Lladó et al. (2014)
Caulobacter flavus RHGG3T Citrullus lanatus 5.65 69.3 4 998 5 175 Yang et al. (2019)
Chryseobacterium kwangjuense Capsicum annum 5.09 38.5 4 445 4 561 Jeong et al. (2016b)
Chryseobacterium sp. GSE06 Cucumis sativus 5.32 36.1 4 658 4 784 Jeong et al. (2016a)
Chryseobacterium sp. ISE14 C. sativus 5.2 36.3 4 482 4 603 Jeong et al. (2018)
Enterobacter aerogenes Cucurbita pepo 5.59 54.93 5 280 5 604 Eevers et al. (2015a)
Enterobacter cloacae GS1 O. sativa 4.5 55.5 3 955 4 053 Shankar et al. (2012)
Enterobacter cloacae SBP-8 Sorghum bicolor 4.85 55 4 055 4 195 Singh et al. (2017)
Enterobacter radicincitans DSM16656T Wheat phyllosphere 6.12 53.72 5 712 5 970 Witzel et al. (2012)
Halolamina pelagica CDK2 Wild grass 2.97 67.6 2 448 3 138 Gaba et al. (2017)
Klebsiella pneumoniae AWD5 Waste-contaminated site 4.8 58.18 4 636 4 824 Rajkumari et al. (2018)
Kosakonia radicincitans YD4 Yerba mate 5.22 54.3 4 758 4 972 Bergottini et al. (2015)
Methylobacterium radiotolerans C. pepo 6.89 71.04 5 690 5 982 Eevers et al. (2015b)
Microbispora sp. GKU 823 Sugarcane 9.43 71.3 7 503 8 902 Kruasuwan et al. (2017a)
Ochrobactrum intermedium SA148 Soil 4.91 57.6 4 502 4 696 Lafi et al. (2017)
Paenibacillus sp. XY044 Camellia sinensis 7.86 52.3 6 979 7 202 Liu et al. (2017)
Pantoea ananatis 1.38 O. sativa 4.86 53.3 4 382 4 644 Megías et al. (2018)
Pantoea ananatis AMG521 O. sativa 4.87 53.1 4 334 4 608 Megías et al. (2016)
Pantoea ananatis B1-9 Green onion 5.1 53.5 4 787 4 622 Kim et al. (2012)
Pantoea sp. 3.5.1 Soil 4.96 55.8 4 423 4 662 Suleimanova et al. (2015)
Pantoea sp. AS-PWVM4 Punica granatum 4.99 54 4 513 4 654 Khatri et al. (2013)
Paraburkholderia tropica P-31 P. granatum 8.9 64.7 7 506 7 827 Kaur et al. (2016)
Preussia sp. BSL10 Tree 31.48 52.8 – – Khan et al. (2016)
Pseudomonas argentinensis SA190 Indigofera argentea 5.07 63.8 4 445 4 611 Lafi et al. (2016)
Pseudomonas lutea OK2T Grasses 5.65 60.2 4 607 4 941 Kwak et al. (2016)
Pseudomonas putida MTCC5279 Cicer arietinum 5.21 62.5 4 579 4 867 Chaudhry et al. (2013)
Pseudomonas viridiflava CDRTc14 Lepidium draba 5.96 59.3 5 245 5 403 Samad et al. (2017)
Pseudomonas sp. CMAA 1215 Soil 6.65 63.8 5 359 6 317 Vasconcellos et al. (2013)
Pseudomonas sp. BMS12 Phragmites karka 4.51 63.94 4 128 – Mishra et al. (2016)
Pseudomonas sp. UW4 Common reed 6.18 60.1 5 447 5 659 Duan et al., (2013)
Rahnella aquatilis HX2 Soil 5.65 52.15 5 012 5 243 Guo et al. (2012)
Raoultella ornithinolytica TNT Soil 5.65 55.5 5 026 5 452 Thijs et al. (2014)
Rhodococcus opacus 04-OD7 Soil 9.32 64.47 8 062 8 886 Zheng et al. (2018)
Serratia fonticola AU-AP2C Pisum sativum 4.99 53.8 4 507 4 677 Devi et al. (2013b)
Serratia fonticola AU-P3(3) P. sativum 5.02 53.8 4 552 4 745 Devi et al. (2013a)
Serratia marcescens RSC-14 S. nigrum 5.12 59.6 4 673 4 849 Khan et al. (2017)
Sphingomonas taxi C. pepo 4.06 67.89 3 620 3 739 Eevers et al. (2015c)
Sphingomonas sp. LK11 Tephrosia apollinea 3.93 66.09 3 450 3 655 Asaf et al. (2018)
Streptomyces sp. GKU 895 Sugarcane 8.2 70.7 6 055 7 758 Kruasuwan et al. (2017b)

antibiotics (Yang et al., 2008), thus providing protection to
plants against soil-borne pathogens (Vassilev et al., 2006).
Phosphate-solubilizing filamentous fungi show biocontrol
activity against Fusarium wilt in tomato, and P. putida also
shows antifungal activity and produces chitinase, β-1,3-
glucanase, salicylic acid, siderophore, and HCN (Khan and
Khan, 2001). Furthermore, in a maize-based bioassay under
greenhouse conditions, it was demonstrated that bacterial
inoculation increases the plant biomass, stimulating bacte-
rial and suppressing fungal abundance in the rhizosphere
(Pandey et al., 2006; Zaidi et al., 2009).
Chang and Yang (2009) reported that thermotolerant P-
solubilizing microbes, such as B. coagulans, B. licheniformis,
B. smithii, B. borstelensis, Streptomyces thermophilus, S.
thermonitrificans, and A. fumigatus, possess different hy-
drolytic enzyme activities, except for S. thermophilus J57,
which lacks pectinase activity. Naik et al. (2008a) observed
that P-solubilizing bacteria, such as P. fulva, P. fluorescens,
P-SOLUBILIZING AND -MOBILIZING MICROBES 61

TABLE V
Diverse sources for and amount of P solubilized by P-solubilizing microbes isolated worldwide
Microbe Host/source Amount of P solubilized Reference
Acetobacter liquefaciens PSB12 Soil 7.29 mg L−1 Joseph and Jisha (2009)
Acetobacter sp. PSB67 Soil 6.38 mg L−1 Joseph and Jisha (2009)
Acetobacter pasteurianus AJK-7 Wheat 8 mg mL−1 Majeed et al. (2015)
Acinetobacter baumannii M05 Mushroom residue 34.88 ± 1.39 µg mL−1 Zhang J et al. (2017)
Acinetobacter sp.a) Solanum nigrum 206.21 ± 3.16 mg L−1 Chen et al. (2010)
Acinetobacter sp. ASL12 Areca catechu 717 ± 12.7 mg L−1 Liu et al. (2014)
Acinetobacter sp. M01 Mushroom residue 54.91 ± 1.25 µg mL−1 Zhang J et al. (2017)
Aspergillus allahabadii D3I8 Asparagus 104.58 ± 4.9 mg L−1 Ruangsanka (2014)
Aspergillus clavatus RHS/P-38 Soil 799 mg mL−1 Chakraborty et al. (2010)
Aspergillus fumigatusb) Soil 93 µg mL−1 Rinu and Pandey (2010)
Aspergillus melleus RS/P-05 Soil 854 mg mL−1 Chakraborty et al. (2010)
Aspergillus niger 1 Soil 285 µg mL−1 Mohan Singh et al. (2011)
Aspergillus niger 2 Soil 262 µg mL−1 Mohan Singh et al. (2011)
Aspergillus niger B1I54 Asparagus 88.93 ± 2.5 mg L−1 Ruangsanka (2014)
Aspergillus niger FS/L-04 Soil 856 mg mL−1 Chakraborty et al. (2010)
Aspergillus nigerb) Soil 1 452 µg mL−1 Rinu and Pandey (2010)
Aspergillus nigerb) Soil 83 µg mL−1 Rinu and Pandey (2010)
Aspergillus wentiib) Soil 21 µg mL−1 Rinu and Pandey (2010)
Azotobacter chroococcum Panax ginseng 863.4 µg mL−1 Hussein and Joo (2015)
Bacillus licheniformisa) Metaphire posthuma 222 ± 2.0 mg L−1 Biswas et al. (2018)
Bacillus megaterium HJR2 Soil 27.4 mg mL−1 Zahid et al. (2015)
Bacillus megaterium M08 Mushroom residue 26.54 ± 1.20 µg mL−1 Zhang J et al. (2017)
Bacillus sp. ADH306 Areca catechu 137 ± 22.9 mg L−1 Liu et al. (2014)
Bacillus sp. HJR7 Soil 28.9 mg mL−1 Zahid et al. (2015)
Bacillus subtilis HJR1 Soil 25.7 mg mL−1 Zahid et al. (2015)
Bacillus megateriuma) M. posthuma 213.7 ± 1.3 mg L−1 Biswas et al. (2018)
Burkholderia sp. QC3.a.1 Soil 50.83 mg L−1 Mursyida et al. (2015)
Candida krissii Phosphate mine 109.3 mg L−1 Xiao et al. (2008)
Ensifer adhaerensb) Rhodiola fastigiata 392.15 mg L−1 Gong et al. (2018)
Enterobacter aerogenesa) S. nigrum 300.60 ± 4.67 mg L−1 Chen et al. (2010)
Enterobacter aerogenes A4 Rice 825.8 µg mL−1 Prasanna et al. (2011)
Enterobacter sp.a) S. nigrum 382.23 ± 4.52 mg L−1 Chen et al. (2010)
Enterobacter sp. ADH302 Areca catechu 426 ± 61.8 mg L−1 Liu et al. (2014)
Enterobacter sp. M03 Mushroom residue 25.66 ± 1.35 µg mL−1 Zhang J et al. (2017)
Escherichia sp. ASG34 A. catechu 499 ± 17.6 mg L−1 Liu et al. (2014)
Klebsiella sp. M02 Mushroom residue 22.94 ± 0.23 µg mL−1 Zhang J et al. (2017)
Kurthia sp. ASG16 Areca catechu 439 ± 7.3 mg L−1 Liu et al. (2014)
Leclercia adecarboxylataa) Soil 218.48 mg L−1 Teng et al. (2019)
Micromonospora sp. AR15 Emblica officinalis 0.38 ± 0.004 mg mL−1 Gangwar et al. (2015)
Mucor ramosissimus Phosphate mine 99.9 mg L−1 Xiao et al. (2008)
Ochrobactrum sp. M11 Mushroom residues 54.41 ± 1.31 µg mL−1 Zhang J et al. (2017)
Paenibacillus sp. ATZ304 A. catechu 266 ± 4.2 mg L−1 Liu et al. (2014)
Paenibacillus taichungensis M10 Mushroom residue 21.34 ± 2.11 µg mL−1 Zhang J et al. (2017)
Penicillium calidicanium A4I9 Asparagus 206.68 ± 3.6 mg L−1 Ruangsanka (2014)
Penicillium expansum Phosphate mines 104.5 mg L−1 Xiao et al. (2008)
Penicillium oxalicum C3I42 Asparagus 556.10 ± 3.7 mg L−1 Ruangsanka (2014)
Penicillium sp. P. ginseng 237.5 µg mL−1 Hussein and Joo (2015)
Pichia farinose FL7 Agricultural waste 436.6 mg L−1 Zhu et al. (2012)
Pseudomonas aeruginosa RB5 Wheat 169.86 µg mL−1 Fouzia et al. (2015)
Pseudomonas fluorescens P. ginseng 885.4 µg mL−1 Hussein and Joo (2015)
Pseudomonas fluorescens CHA0 Wheat 50.08 µg mL−1 Fouzia et al. (2015)
Pseudomonas fluorescens RB13 Wheat 187.9 µg mL−1 Fouzia et al. (2015)
Pseudomonas gladioli PSB 73 Soil 6.88 mg L−1 Joseph and Jisha (2009)
Pseudomonas putida QC3.d.5 Soil 43.22 mg L−1 Mursyida et al. (2015)
Pseudomonas sp. P34-L Wheat 101.6 µg mL−1 Liu et al. (2018)
Pseudomonas stutzeri MR6 Soil 19.2 mg mL−1 Zahid et al. (2015)
Rhizobium sp. AX7 A. catechu 275 ± 45.7 mg L−1 Liu et al. (2014)
Serratia marcescens SRM Cucurbita pepo 76.6 µg mL−1 Selvakumar et al. (2008)
Serratia nematodiphilaa) S. nigrum 258.56 ± 5.44 mg L−1 Chen et al. (2010)
Serratia sp. QC3.a.2 Soil 80.61 mg L−1 Mursyida et al. (2015)
Shigella sp. ASG33 A. catechu 530 ± 53.2 mg L−1 Liu et al. (2014)
Sphingobacterium sp. M13 Mushroom residue 21.64 ± 1.11 µg mL−1 Zhang J et al. (2017)
Staphylococcus haemolyticusa) M. posthuma 193.5 ± 1.5 mg L−1 Biswas et al. (2018)
(to be continued)
62
TABLE V (continued)
Microbe Host/source
Stenotrophomonas rhizophila AJK-3 Wheat
Stenotrophomonas sp. AJK-9 Wheat
Streptomyces tricolor mhce0811 Wheat
Streptomyces cellulosae mhcr0816 Wheat
Streptomyces cinereus AR3 E. officinalis
Streptomyces griseofuscus AL4 E. officinalis
Talaromyces funiculosusc) Neem
Trichoderma sp. DRT-I Cedrus deodara
a) Heavy metal-resistant.
b) Low temperature-resistant.
c) Salinity-resistant.
P. mosselii, P. monteilii, P. plecoglossicida, and P. putida,
produce siderophores, some show the production of IAA,
ACC deaminase, chitinase, pectinase, and cellulase, and
some have both proteolytic and antifungal activities. Sel-
vakumar et al. (2009) found that E. acetylicum (1P) isolated
from the rhizosphere of Malus domestica shows growth from
at temperature from 4 to 42 ◦ C, can tolerate pH from 4 to 10
and up to 8% salt, produces IAA, HCN, and siderophores
simultaneously at 4 ◦ C, and shows P-solubilizing ability at
this suboptimal temperature.
The phytase-producing and P-solubilizing bacteria
Achromobacter sp., Tetrathiobacter sp., and Bacillus sp.
can grow at wide ranges of pH, temperature, and salt and
produce IAA and siderophores (Kumar V et al., 2013).
Bumunang and Babalola (2014) screened the rhizobacteria
isolated from genetically and non-genetically modified maize
for various plant growth-promoting attributes, including P
solubilization, ammonia production, catalase activity, IAA
production, HCN production, and antifungal activity, and
found that 90.6% of the isolates are P solubilizers: those
isolated from genetically modified maize, B. cepacia, P. lu-
teola, S. maltophilia, P. putida, and S. paucimobilis, all show
IAA, ammonia, and catalase production, with some sho-
wing antifungal activity; those isolated from non-genetically
modified maize, A. xylosoxidans, B. safensis, B. cepacia,
E. americana, P. stutzeri, P. putida, S. paucimobilis, and S.
maltophilia, all produce IAA, ammonia, and catalase, with
two showing antifungal activity.
Chauhan et al. (2017) reported that the P-solubilizing
A. aneurinilyticus CKMV1 shows multiple plant growth-
promoting traits, such as N fixation, the production of IAA,
siderophores, and HCN, and antifungal activity against Al-
ternaria sp., Dematophora necatrix, F. oxysporum, Phytoph-
thora sp., R. solani, and Sclerotium rolfsii. Afzal et al. (2017)
isolated endophytic bacteria, belonging to the genera Agro-
coccus, Bacillus, Brevundimonas, Inquilinus, Microbac-
terium, Pseudomonas, Rhizobium, Stenotrophomonas, Strep-
tomyces, and Xanthomonas, from Dodonaea viscose; they
found that some of the isolates solubilize P and produce
cellulase, pectinase, protease, siderophores, HCN, and ACC
D. KOUR et al.
Amount of P solubilized Reference
16 mg mL−1 Majeed et al. (2015)
4 mg mL−1 Majeed et al. (2015)
950 ± 09 mg L−1 Jog et al. (2014)
1916 ± 10 mg L−1 Jog et al. (2014)
0.45 ± 0.004 mg mL−1 Gangwar et al. (2015)
0.38 ± 0.004 mg mL−1 Gangwar et al. (2015)
187 mg L−1 Kanse et al. (2015)
404.07 µg mL−1 Kapri and Tewari (2010)
deaminase and some show antifungal activity, with all iso-
lates being IAA and ammonia producers. Sánchez-Cruz
et al. (2019) isolated Serratia sp. and Enterobacter sp.
from Mimosa pudica root nodules; they found that these
bacteria possess P-solubilizing capabilities and other plant
growth-promoting attributes, including the production of
IAA, siderophores, chitinase, and cellulase, as well as N
fixation. Singh et al. (2019) isolated A. calcoaceticus, Azo-
tobacter sp., Bacillus aerius, B. amyloliquefaciens, Bacillus
mucilaginous, B. subtilis, Ralstonia sp., and S. maltophilia
from Momordica charantia; they found that these strains
all possess P-solubilizing capabilities and produce IAA and
ammonia and some of them also produce siderophores and
HCN.
Role of P-solubilizing microbes in crop improvement
To increase the growth and yield of crops, large amounts
of chemical fertilizers are demanded. However, the increases
in the costs of these chemical fertilizers and environmen-
tal concerns regarding them have led to the development
of alternative strategies, i.e., the use of beneficial soil mi-
crobes. Thus, P-solubilizing microbes with diverse plant
growth-promoting attributes can be used as inoculants for
the mobilization of P from poorly available sources in soil.
Thus, screening potential P-solubilizing isolates and using
them as bioinoculants to increase plant growth and yield is
recognized as an area of interest.
Inoculating crops with P-solubilizing microbes
Extensive studies have been performed to demonstrate
the effect of inoculating of crops with P-solubilizing bacteria
and fungi isolated from different environments. Of these, the
pseudomonads are by far the most pertinent cold-tolerant
P solubilizers that have been identified and tested so far,
followed by species of Bacillus. These cold-tolerant P solu-
bilizers possess attractive traits, for instance, N fixation and
antagonism against phytopathogens (Pandey et al., 2006;
Mishra et al., 2008; Bashan et al., 2016). Accordingly, the
growth-promoting capabilities of Pseudomonas isolates have
been tested on an array of crops, including mung bean,
P-SOLUBILIZING AND -MOBILIZING MICROBES
wheat, rice, and lentil (Egamberdiyeva and Höflich, 2003;
Katiyar and Goel, 2003; Trivedi and Sa, 2008; Mishra et al.,
2008, 2009; Selvakumar et al., 2011). Cold-tolerant Bacillus
strains have also been used to promote the growth of lentil,
rice, millet, and Indian mustard (Malviya et al., 2012; Kumar
V et al., 2013).
The improved growth of C. arietinum and Hordeum
vulgare, as well as increased N and P contents in them,
has been observed after inoculation with Mesorhizobium
mediterraneum possessing N2 -fixing as well as P-solubilizing
capabilities, with further improvements after concomitant
application of M. mediterraneum and Ca3 (PO4)2 (Peix et al.,
2001). Wakelin et al. (2004, 2005) reported that inoculation
with P. radicum increase wheat growth on neutral-to-alkaline
sandy soils. Duponnois et al. (2006) observed an increase
in the P uptake and shoot dry weight of Acacia holosericea
when inoculated with the fungus A. oligospora, with further
increase in plant P uptake and growth after addition of rock
phosphate with P-solubilizing microbes. Shin et al. (2006)
reported that inoculation with P. oxalicum, either alone or
with fused phosphates and rock phosphate, increases the
growth and N and P contents of Zea mays plants. Gane-
san (2008) reported that inoculation with P. aeruginosa, a
cadmium-resistant P solubilizer with other plant growth-
promoting traits, reduces metal toxicity in black gram grown
on soil treated with a gradient of CdCl2 concentrations. Ekin
(2010) showed that inoculation with P-solubilizing Bacillus
sp. improves the P mobilization in sunflower, as well as the
seed quality and oil yield.
Viruel et al. (2014) studied the effect of inoculation with
P-solubilizing bacteria, such as E. aerogenes, P. agglomerans,
Pantoea eucalypti, Pseudomonas koreensis, Pseudomonas
tolaasii, and S. marcescens, on the growth and yield of
maize. They found significant increases in height and shoot
dry weight, as well as P content, of plants treated with P.
tolaasii compared to those of the uninoculated control. The
study of Midekssa et al. (2015) indicates that inoculation with
Bacillus sp., B. subtilis, Enterobacter kobei, Enterobacter sp.,
and P. fluorescens improve the growth, nodulation, and N and
P contents of lentil shoots. Chauhan et al. (2017) isolated
the P-solubilizing rhizobacterial strain A. aneurinilyticus
CKMV1 from V. jatamansi, characterized its production
of IAA, siderophores, and HCN, as well as its antifungal
activity, and assessed its plant growth-promoting traits using
tomato under net house conditions. They observed significant
increases in seed germination, shoot length, root length, shoot
dry weight, and root dry weight, along with N, P, and K
contents. Hassan et al. (2017) observed increases in the plant
height, branches per plant, leaves per plant, pods per plant,
seeds per plant, pod length, 1 000-seed weight, number
of effective nodules, nodule density, chlorophyll a and b
contents, carotenoid content, protein content, and proline
63
content of mung bean inoculated with two P solubilizers, B.
polymyxa and Pseudomonas striata, with increased P and N
contents in soil and the uptake of macronutrients, including
N, P, K, Ca, and Mg, in the roots and shoots of the plant,
compared to those in the non-inoculated control.
Inoculating crops with consortia of P-solubilizing microbes
There are several reports on the application of P-
solubilizing microbes in agronomic practices, either in-
dividually or in combination, to assess their effects on the
growth and biomass production of several crops (Table VI). A
biofertilizer product under the trade name Phosphobacterin,
which actually contains B. megaterium var.phosphaticum,
has soon been introduced to Eastern Europe and India after
its commercialization in former Soviet Union (Khan et al.,
2007). Similarly, a consortium with efficient P solubilizers,
such as P. striata, B. polymyxa, Aspergillus awamori, A.
niger, and Penicillium digitatum, termed the Indian Agri-
cultural Research Institute (IARI) microphos culture (Gaur,
1990), was developed in India (Khan et al., 2010).
Chlorophyll content in barley increases after applica-
tion of mycorrhiza along with P. putida (Bartholdy et al.,
2001). Barea et al. (2002) reported an increased P uptake in
several legumes fertilized with rock phosphate and inocu-
lated with P-solubilizing rhizobacteria, mycorrhizal fungi,
and Rhizobium in combination. Son et al. (2006) studied
the effect of inoculation with Bradyrhizobium japonicum
and P-solubilizing bacteria Pseudomonas sp. with different
rates of inorganic N fertilizer and biofertilizer on soybean
in rotational system. Akhtar and Siddiqui (2009) studied
the effects of P-solubilizing microorganisms, A. awamori,
G. intraradices, P. aeruginosa, P. alcaligenes, P. putida,
and Rhizobium sp., on the growth, nodulation, yield, and
root-rot disease complex of chickpea under field conditions
and found root galling was reduced mostly by inoculation
with P. putida followed by P. aeruginosa, P. alcaligenes, G.
intraradices, and A. awamori, with Rhizobium sp. showing a
similar reduction in galling to P. putida.
Malviya et al. (2011) reported that inoculation of ground
nut (Arachis hypogaea) plants with the P-solubilizing fungi
A. niger and Penicillium notatum in combination significantly
increases the dry matter, yield, protein and oil percentages,
and N and P contents of ground nut plants. The inoculation
with P-solubilizing bacteria B. megaterium along with the po-
tential N-fixer Azotobacter sp. can induce resistance against
the harmful effects of salinity while simultaneously impro-
ving the growth and yield of wheat (Krishnaraj and Dahale,
2014). The inoculation of foxtail millet with A. lipoferum and
P-solubilizing bacteria alone or in combination can increase
the plant height, root and shoot dry weights, and panicle and
seed weights (Rafi et al., 2017). The inoculation of mung
bean with the P-solubilizing isolates P. agglomerans PSB-1
64
TABLE VI
Multifarious plant growth-promoting attributes of P-solubilizing microbes
Microbe
Actinobacteria
Acinetobacter calcoaceticus
Acinetobacter lwoffii/johnsonii
Acinetobacter baumannii
Acinetobacter sp.
Acinetobacter rhizosphaerae
Streptomyces sp.
Microbispora sp.
Streptomyces sp.
Clavibacter michiganensis
Kitasatospora sp.
Acinetobacter calcoaceticus
Firmicutes
Bacillus altitudinis
Bacillus megaterium
Bacillus licheniformis
Bacillus sp.
Bacillus sp.
Bacillus sp.
Paenibacillus taichungensis
Bacillus sp.
Staphylococcus lentus
Staphylococcus aureus
Bacillus pumilus
Bacillus simplex
Paenibacillus taichungensis
Paenibacillus sp.
Bacillus cereus
Bacillus thuringiensis
Bacillus pumilis
Bacillus sp.
Paenibacillus sp.
Enterococcus casseliflavus
Enterococcus gallinarum
Bacillus sp.
Bacillus subtilis
Bacillus amyloliquefaciens
Bacillus mucilaginous
Bacillus aerius
Hallobacillus sp.
Proteobacteria
Serratia marcescens
Pseudomonas sp.
Burkholderia sp.
Pseudomonas baetica
Serratia liquefaciens
Pseudomonas vancouverensis
Enterobacter sp.
Roseomonas sp.
Pantoea sp.
Pseudomonas putida
Enterobacter sp.
Pantoea sp.
Achromobacter sp.
Achromobacter xylosoxidans
Pseudomonas sp.
Pseudomonas aeruginosa
Rhizobium panacihumi
Enterobacter sp.
Pseudomonas sp.
Stenotrophomonas maltophilia
Ralstonia sp.
Ensifer adhaerens
D. KOUR et al.
Increased content N2 fixation Productiona) Reference
P K Zn IAA GA ACCD Sid
+b) + + Sarode Prashant et al. (2009)
+ + + + Toribio-Jiménez et al. (2017)
+ + Zhang J et al. (2017)
+ + + Rokhbakhsh-Zamin et al. (2011)
+ + + + Gulati et al. (2009)
+ + + Jog et al. (2014)
+ + + Kruasuwan and Thamchaipenet (2016)
+ + + + Kruasuwan and Thamchaipenet (2016)
+ + Kumar A et al. (2016b)
+ + Tchakounté et al. (2018)
+ + + Singh et al. (2019)
+ + + Sunar et al. (2015)
+ + + Zhang J et al. (2017)
+ + + + Pahari and Mishra (2017)
+ + + Iqbal Hussain et al. (2013)
+ + + Zhang J et al. (2017)
+ + Shahid et al. (2015)
+ + + Zhang J et al. (2017)
+ Rana et al. (2011)
+ + + Toribio-Jiménez et al. (2017)
+ + + Toribio-Jiménez et al. (2017)
+ + + Zhang et al. (2018)
+ + Zhang et al. (2018)
+ + + Zhang J et al. (2017)
+ + + Kruasuwan and Thamchaipenet (2016)
+ + Kumar A et al. (2016b)
+ + Kumar A et al. (2016b)
+ + Kumar A et al. (2016b)
+ + + Batista et al. (2018)
+ + + Tchakounté et al. (2018)
+ + Mussa et al. (2018)
+ + Mussa et al. (2018)
+ + Verma et al. (2018)
+ + + Singh et al. (2019)
+ + + Singh et al. (2019)
+ + + Singh et al. (2019)
+ + + Singh et al. (2019)
+ + + + Ramadoss et al. (2013)
+ + Selvakumar et al. (2008)
+ + Liu et al. (2018)
+ + + + Usha et al. (2015)
+ + + Zhang et al. (2018)
+ + Zhang et al. (2018)
+ + Zhang et al. (2018)
+ + + + + Kruasuwan and Thamchaipenet (2016)
+ + Tchakounté et al. (2018)
+ + Kruasuwan and Thamchaipenet (2016)
+ + + Kumar A et al. (2016b)
+ + Leite et al. (2018)
+ + Leite et al. (2018)
+ + Leite et al. (2018)
+ + Vyas et al. (2018)
+ + + Lakra and Mishra (2018)
+ + + Uzair et al. (2018)
+ + + Kang et al. (2019)
+ + Verma et al. (2018)
+ + Verma et al. (2018)
+ + + Singh et al. (2019)
+ + Singh et al. (2019)
+ + + Gong et al. (2018)
(to be continued)
P-SOLUBILIZING AND -MOBILIZING MICROBES 65

TABLE VI (continued)
Microbe
Pseudomonas luteola
Burkholderia cepacia
Burkholderia gladioli
Sphingomonas paucimobilis
Aeromonas hydrophila
Enterobacter sp.
Providencia sp.
Brevundimonas diminuta
Pseudomonas koreenis
Pseudomonas alcaliphila
Ochrobactrum pituitosum
Bacteroidetes
Sphingobacterium sp.
Ascomycota
Arthroderma cuniculi
Aspergillus niger
Curvularia geniculata
Fusarium proliferatum
Trichoderma harzianum
Lecanicillium psalliotae
Penicillium menonorum
Aureobasidium pullulans
Candida sp.
Dothideomycetes sp.
Hanseniaspora uvarum
Meyerozyma caribbica
Saccharomyces cerevisiae
Torulaspora sp.
Barnettozyma californica
Trichoderma gamsii
Basidiomycota
Cryptococcus laurentii
Pseudozyma aphidis
Rhodosporidium paludigenum
Sporidiobolus ruineniae
Ustilago esculenta
Pseudozyma rugulosa
a) IAA = indole-3-acetic acid; GA = gibberellic acid; ACCD = 1-aminocyclopropane-1-carboxylate (ACC) deaminase; Sid = siderophore.
b) Positive result.
Increased content N2 fixation Productiona) Reference
P K Zn IAA GA ACCD Sid
+ + + Martínez-Gallegos et al. (2018)
+ + + Martínez-Gallegos et al. (2018)
+ + + Martínez-Gallegos et al. (2018)
+ + + Martínez-Gallegos et al. (2018)
+ + + Martínez-Gallegos et al. (2018)
+ + + Martínez-Gallegos et al. (2018)
+ + + + + Rana et al. (2011)
+ Rana et al. (2011)
+ + + Zhang et al. (2018)
+ + + Zhang et al. (2018)
+ + + Zhang et al. (2018)
+ Zhang J et al. (2017)
+ + Karmakar et al. (2018)
+ + Wang et al. (2018)
+ + Priyadharsini and Muthukumar (2017)
+ + + Bilal et al. (2018)
+ + Altomare et al. (1999)
+ + + Kumar et al. (2018)
+ + + Babu et al. (2015)
+ + + + Fu et al. (2016)
+ + + Fu et al. (2016)
+ + + + Fu et al. (2016)
+ + Fu et al. (2016)
+ + Fu et al. (2016)
+ + Fu et al. (2016)
+ + + Fu et al. (2016)
+ + + Fu et al. (2016)
+ Rinu et al. (2014)
+ + + Fu et al. (2016)
+ + + Fu et al. (2016)
+ + Fu et al. (2016)
+ + + Fu et al. (2016)
+ + Fu et al. (2016)
+ + Fu et al. (2016)

and Burkholderia anthina PSB-2 would enhance the shoot
and root lengths, shoot and root dry matter, and P uptake of
the plant (Charana Walpola and Yoon, 2013). The synergistic
effect of the P-solubilizing bacteria P. fluorescens and B.
cepacia with the AM fungus G. etunicatum was studied
using wheat plants grown in pots with nutrient-deficient
soils and amended with TCP, and significant increases in
the growth, yield, and nutrient uptake of the plants were
observed (Minaxi et al., 2013).
Maize inoculated with Bacillus sp., Burkholderia sp.,
and Flavobacterium sp. shows significant increases in plant
height, biomass, root length, and grain yield, compared to the
uninoculated control (Iqbal Hussain et al., 2013). Nandini
et al. (2014) isolated P-solubilizing A. faecalis from the
rhizospheric soil of upland rice and further studied the effect
of the isolate alone or in combination with B. megaterium
and B. japonicum on soybean growth. They found increases
in plant height, number of leaves, number of pods, dry
weight, and grain yield of the inoculated plants compared
to the control plants. Saxena et al. (2014) evaluated the
synergistic effect of the AM fungus G. etunicatum with
the indigenous P-solubilizing bacterial strain B. cepacia
on wheat plants. They found that dual inoculation with
G. etunicatum and B. cepacia increases all studied growth
and yield parameters compared to individual inoculations.
Roy et al. (2017) studied the individual and synergetic
effects of the free-living diazotrophic bacteria A. brasilense,
Azotobacter chroococcum, and Clostridium pasteurianum
with the P-solubilizing bacteria Pseudomonas denitrificans
and Rhizobium sp. on the growth of rice cultivar NDR-
359. They reported that inoculated strains, both individually
and in combination, increase the shoot length, number of
tillers per plant, number of leaves per tiller, root length, and
root volume.
CONCLUSIONS
Most of the soils worldwide are deficient in plant-
available P; this necessitates the use of expensive P fertilizers.
66
Thus, scientists and microbiologists are greatly focusing on
finding alternate solutions to this P deficiency. There is a huge
diversity of microbes in soil, some of which have already
been reported and some of which remain to be explored,
for their capability to solubilize P and make it available
to plant. Generally, P-solubilizing microbes also possess
other plant growth-promoting attributes, including the pro-
duction of various plant growth regulators, siderophores,
HCN, ammonia, and hydrolytic enzymes; these compounds
also protect the plants from various abiotic stresses. Thus,
these plant growth-promoting P-solubilizing microbes can
be used as biofertilizers, not only to promote the plant growth
or increase P availability, but also to restore soil fertility and
reduce the use of chemical fertilizers, which is the key to sus-
tainable agriculture. The combined inoculation of AM fungi
with P-solubilizing microbes can make native soil P available
to plant. However, further research is needed to evaluate the
P-solubilizing stability and performance of both natural and
genetically modified strains applied to soil-plant systems.
The understanding of the genetics behind the solubilization
of P is important, and chromosomal insertion of the PQQ
synthase gene would be beneficial. Finally, it is very essential
that researchers and microbiologists continue to learn about
P-solubilizing microbes and transfer their knowledge into
bio-based inoculants that could be made easily available to
farmers; awareness must also be created among farmers to
use inoculants that make sustainable agriculture possible.
CONTRIBUTION OF AUTHORS
Divjot Kour and Kusam Lata Rana contributed equally
to this review.
ACKNOWLEDGMENTS
The authors are grateful to the Department of Biote-
chnology, Akal College of Agriculture, Eternal University
and the Department of Environment, Science & Technology
(DEST), India-funded project “Development of Microbial
Consortium as Bio-inoculants for Drought and Low Tem-
perature Growing Crops for Organic Farming in Himachal
Pradesh” for providing the facilities and financial support
to undertake the investigations. There are no conflicts of
interest.
SUPPLEMENTARY MATERIAL
Supplementary material for this article can be found in
the online version.
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