Phosphate-Solubilizing Microorganisms in Sustainable Agriculture: Genetic Mechanism and Application

  • A. Pradhan
  • A. Pahari
  • S. Mohapatra
  • Bibhuti Bhusan MishraEmail author
Part of the Microorganisms for Sustainability book series (MICRO, volume 4)


Phosphorus (P) is the second important nutrient in terms of plant requirement and uptake. Though it is present in the soil in both organic and inorganic forms, its accessibility is constrained as it occurs mostly in insoluble forms. Additional requirement of P to satisfy nutritional requirements of the crop is usually supplemented as chemical P fertilizer. A number of soil microorganisms named phosphate-solubilizing microorganisms (PSMs) have been tested for solubilizing/mineralizing insoluble soil P, releasing in soluble form and making it available for plant uptake. PSMs are environment-friendly and deliver P to plants in a more sustainable manner. The present chapter focuses on the biochemical, molecular, and genetic mechanisms of P release by different PSMs. Phosphorus solubilization through diffusion of strong organic acids produced in the periplasm of the organism, into the adjacent soil environment, is one of the important mechanisms for P solubilization and is genetically controlled. The use of PSM is a promising approach to develop and fulfill P demand of the growing crop without causing any environmental hazard.


Phosphate-solubilizing microorganisms (PSMs) P-solubilizing bacteria Organic acid Genetics of P solubilization Biofertilizer 


  1. Adhya TK, Kumar N, Reddy G, Podile RA, Bee H, Samantaray B (2015) Microbial mobilization of soil phosphorus and sustainable P management in agricultural soils. Special section: sustainable phosphorus management. Curr Sci 108(7):1280–1287Google Scholar
  2. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20CrossRefGoogle Scholar
  3. Anthony OA, Kloepper JW (2009) Appl Microbiol Biotechnol 85:1–12CrossRefGoogle Scholar
  4. Atlas R, Bartha R (1997) Microbial ecology. Addison Wesley Longman, New YorkGoogle Scholar
  5. Babu-Khan S, Yeo TC, Martin WL, Duron MR, Rogers RD, Goldstein AH (1995) Cloning of a mineral phosphate-solubilizing gene from Pseudomonas cepacia. Appl Environ Microbiol 61:972–678PubMedPubMedCentralGoogle Scholar
  6. Banik S, Dey BK (1982) Available phosphate content of an alluvial soil as influenced by inoculation of some isolated phosphate solubilizing microorganisms. Plant Soil 69:353–364CrossRefGoogle Scholar
  7. Beech IB, Paiva M, Caus M, Coutinho C (2001) Enzymatic activity and within biofilms of sulphate-reducing bacteria. In: Gilbert PG, Allison D, Brading M, Verran J, Walker J (eds) Biofilm community interactions: change or necessity? Boiline, Cardiff, pp 231–239Google Scholar
  8. Begon M, Harper JL, Townsend CR (1990) Ecology: individuals, populations and communities, 2nd edn. Blackwell Scientific Publications, BostonGoogle Scholar
  9. Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Factories 13:66CrossRefGoogle Scholar
  10. Bhargava T, Datta S, Ramachandran V, Ramakrishnan R, Roy RK, Sankaran K, Subrahmanyam YVBK (1995) Virulent Shigella codes for a soluble apyrase: identification, characterization and cloning of the gene. Curr Sci 68:293–300Google Scholar
  11. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting Rhizobacteria PGPR: emergence in agriculture. J World Microbiol Biotechnol 28:1327–1350CrossRefGoogle Scholar
  12. Bishop ML, Chang AC, Lee RWK (1994) Enzymatic mineralization of organic phosphorus in a volcanic soil in Chile. Soil Sci 157:238–243CrossRefGoogle Scholar
  13. Childers DL, Corman J, Edwards M, Elser JJ (2011) Sustainability challenges of phosphorus and food: solutions from closing the human phosphorus cycle. Bioscience 61:117–124CrossRefGoogle Scholar
  14. Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305CrossRefGoogle Scholar
  15. Daniel P, Schachtman RJR, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453CrossRefGoogle Scholar
  16. De Weger LA, van der Bij AJ, Dekkers LC, Simons M, Wijffelman CA, Lugtenberg BJJ (1995) Colonization of the rhizosphere of crop plants by plant-beneficial pseudomonads. FEMS Microbiol Ecol 17:221–228CrossRefGoogle Scholar
  17. Elizabeth T, Alori GBR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol.
  18. Fankem H, Nwaga D, Deube A, Dieng L, Merbach W, Etoa FX (2006) Occurrence and functioning of phosphate solubilizing microorganisms from oil palm tree (Elaeis guineensis) rhizosphere in Cameroon. Afr J Biotechnol 5:2450–2460Google Scholar
  19. FAOSTAT (2012) Last access date 02/05/2012
  20. Fraga R, Rodriguez H, Gonzalez T (2001) Transfer of the gene encoding the Nap A acid phosphatase from Morganella morganii to a Burkholderia cepacia strain. Acta Biotechnol 21:359–369CrossRefGoogle Scholar
  21. Furihata T, Suzuki M, Sakuri H (1992) Kinetic characterization of two phosphate uptake systems with different affinities in suspension cultured Catharan roseus protoplasts. Plant Cell Physiol 33:1151–1157Google Scholar
  22. Gaur AC (1990) Phosphate solubilizing microorganisms as biofertilizers. Omega Scientific Publisher, New Delhi, p 176Google Scholar
  23. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
  24. Goldstein AH (1986) Bacterial solubilization of mineral phosphates: historical perspective and future prospects. Am J Altern Agric 1:51–57CrossRefGoogle Scholar
  25. Goldstein AH (1996) Involvement of the quinoprotein glucose dehydrogenase in the solubilization of exogenous phosphates by Gram-negative bacteria. In: Torriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 197–203Google Scholar
  26. Goldstein AH, Liu ST (1987) Molecular cloning and regulation of a mineral phosphate solubilizing gene from Erwinia herbicola. Biotechnology 5:72–74Google Scholar
  27. Goldstein AH, Rogers RD, Mead G (1993) Mining by microbe. Biotechnology 11:1250–1254Google Scholar
  28. Goosen N, Horsman HPA, Huinen RG, van de Putte P (1989) Acinetobacter calcoaceticus genes involved in biosynthesis of the coenzyme pyrrolo-quinoline- quinine: nucleotide sequence and expression in Escherichia coli k-12. J Bacteriol 171:447–455CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gügi B, Orange N, Hellio F, Burini JF, Guillou C, Leriche F, Guespin-Michel JF (1991) Effect of growth temperature on several exported enzyme activities in the psychrotropic bacterium Pseudomonas fluorescens. J Bacteriol 173:3814–3820CrossRefPubMedPubMedCentralGoogle Scholar
  30. Halder AK, Chakrabartty PK (1993) Solubilization of inorganic phosphate by Rhizobium. Folia Microbiol 38:325–330CrossRefGoogle Scholar
  31. Halder AK, Mishra AK, Bhattacharyya P, Chakrabartty PK (1990) Solubilization of rock phosphate by Rhizobium and Bradyrhizobium. J Gen Appl Microbiol 36:81–92CrossRefGoogle Scholar
  32. Hilda R, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339CrossRefGoogle Scholar
  33. Houck DR, Hanners JL, Unkefer CJ (1991) Biosynthesis of pyrroloquinoline quinone. Biosynthetic assembly from glutamate and tyrosine. J Am Chem Soc 113:3162–3166CrossRefGoogle Scholar
  34. Illmer P, Schinner F (1992) Solubilization of inorganic phosphates by microorganisms isolated from forest soil. Soil Biol Biochem 24:389–395CrossRefGoogle Scholar
  35. Kloepper JW, Lifshitz R, Zablotowitz RM (1989) Free living bacteria inocula for enhancing crop productivity. Trends Biotechnol 7:39–43CrossRefGoogle Scholar
  36. Kucey RMN, Janzen HH, Legett ME (1989) Microbially mediated increases in plant-available phosphorus. Adv Agron 42:198–228Google Scholar
  37. Kumar V, Singh P, Jorquera MA, Sangwan P, Kumar P, Verma AK, Sanjeev A (2013) Isolation of phytase-producing bacteria from Himalayan soils and their effect on growth and phosphorus uptake of Indian mustard (Brassica juncea). World J Microbiol Biotechnol 29:1361–1369CrossRefPubMedGoogle Scholar
  38. Liu TS, Lee LY, Tai CY, Hung CH, Chang YS, Wolfram JH, Rogers R, Goldstein AH (1992) Cloning of an Erwinia herbicola gene necessary for gluconic acid production and enhanced mineral phosphate solubilization in Escherichia coli HB101: nucleotide sequence and probable involvement in biosynthesis of the coenzyme pyrroloquinoline quinone. J Bacteriol 174:5814–5819CrossRefPubMedPubMedCentralGoogle Scholar
  39. Maliha R, Samina K, Najma A, Sadia A, Farooq L (2004) Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms under in vitro conditions. Pak J Biol Sci 7:187–196CrossRefGoogle Scholar
  40. Maougal RT, Brauman A, Plassard C, Abadie J, Djekoun A, Drevon JJ (2014) Bacterial capacities to mineralize phytate increase in the rhizosphere of nodulated common bean (Phaseolus vulgaris) under P deficiency. Eur J Soil Biol 62:8–14CrossRefGoogle Scholar
  41. McGrath JW, Wisdom GB, McMullan G, Larkin MJ, Quinn JP (1995) The purification and properties of phosphonoacetate hydrolase, a novel carbon-phosphorus bond-cleavage enzyme from Pseudomonas fluorescens 23F. Eur J Biochem 234:225–230CrossRefPubMedGoogle Scholar
  42. Meulenberg JJM, Sellink E, Loenen WAM (1990) Cloning of Klebsiella Pneumoniae pqq genes and PQQ biosynthesis in Escherichia coli. FEMS Microbiol Lett 71:337–343CrossRefGoogle Scholar
  43. Meulenberg JJ, Sellink E, Riegman NH, Postma PW (1992) Nucleotide sequence and structure of the Klebsiella pneumoniae pqq operon. Mol Gen Genet 232:284–294PubMedGoogle Scholar
  44. Mohammad SK, Zaidi A, Parvaze AW (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture – a review. Agron Sustain Dev 27(1):29–43. SpringerCrossRefGoogle Scholar
  45. Morris CJ, Biville F, Turlin E, Lee E, Ellermann K, Fan WH, Ramamoorthi R, Springer AL, Lidstrom ME (1994) Isolation, phenotypic characterization, and complementation analysis of mutants of Methylobacterium extorquens AM1 unable to synthesize pyrroloquinoline quinone and sequences of pqqD, pqqG, and pqqC. J Bacteriol 176(6):1746–1755CrossRefPubMedPubMedCentralGoogle Scholar
  46. Motsara MR (2002) Phosphorus fertility status of soils in India. Fertil News 47:15–21Google Scholar
  47. Muralidharudu Y, Reddy SK, Mandal BN, Rao SA, Singh KN, Sonekar S (2011) GIS based soil fertility maps of different states of India. AICRP-STCR, IISS, Bhopal, p 224Google Scholar
  48. Nozawa M, HY H, Fujie K, Tanaka H, Urano K (1998) Quantitative detection of Enterobacter cloacae strain HO-I in bioreactor for chromate wastewater treatment using polymerase chain reaction [PCR]. Water Resour Manag 32:3472–3476Google Scholar
  49. Ohtake H, Wu H, Imazu K, Anbe Y, Kato J, Kuroda A (1996) Bacterial phosphonate degradation, phosphite oxidation and polyphosphate accumulation. Res Cons Recy 18:125–134CrossRefGoogle Scholar
  50. Oliveira CA, Sa NMH, Gomes EA, Marriel IE, Scotti MR, Guimaraes CT, Schaffert RE, Alves VMC (2009) Assessment of the mycorrhizal community in the rhizosphere of maize (Zea mays L.) genotypes contrasting for phosphorus efficiency in the acid savannas of Brazil using denaturing gradient gel electrophoresis (DGGE). Appl Soil Ecol 41:249–258CrossRefGoogle Scholar
  51. Omar SA (1998) The role of rock phosphate solubilizing fungi and vesicular arbuscular mycorrhiza (VAM) in growth of wheat plants fertilized with rock phosphate. World J Microbiol Biotechnol 14:211–219CrossRefGoogle Scholar
  52. Paul EA, Clark FE (1988) Soil microbiology and biochemistry. Academic, San DiegoGoogle Scholar
  53. Pradhan A, Baisakh B, Mishra BB (2014) Plant growth characteristics of bacteria isolated from rhizosphere region of Santalum album. J Pure Appl Microbiol 8(6):4775–4781Google Scholar
  54. Ramamurthy B, Bajaj JC (1969) Available nitrogen, phosphorus and potassium status of Indian soils. Fertil News 14:25–36Google Scholar
  55. Richardson AE (1994) Soil microorganisms and phosphorus availability. In: Pankhurst CE, Doube BM, Gupta VVSR, Grace PR (eds) Soil biota, management in sustainable farming systems. CSIRO, Melbourne, pp 50–62Google Scholar
  56. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906Google Scholar
  57. Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas spp. that utilize inositol phosphates. Can J Microbiol 43:509–516CrossRefPubMedGoogle Scholar
  58. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996CrossRefPubMedPubMedCentralGoogle Scholar
  59. Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339CrossRefPubMedGoogle Scholar
  60. Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21CrossRefGoogle Scholar
  61. Rosenberg H (1987) Phosphate transport in prokaryotes. In: Rosen B, Silver S (eds) Ion transport in prokaryotes. Academic, San Diego, pp 205–248CrossRefGoogle Scholar
  62. Ross HM (2013) Phosphorus fertilizer application in crop production Agri-facts. Practical information for Alberta’s agriculture industry, pp 1–12Google Scholar
  63. Saber K, Nahla LD, Chedly A (2005) Effect of P on nodule formation and N fixation in bean. Agron Sustain Dev 25:389–393CrossRefGoogle Scholar
  64. Salimpour S, Khavazi K, Nadian H, Besharati H, Miransari M (2010) Enhancing phosphorous availability to canola (Brassica napus L.) using P solubilizing and sulfur oxidizing bacteria. Aust J Crop Sci 4:330–334Google Scholar
  65. Santos-Beneit (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:402CrossRefPubMedPubMedCentralGoogle Scholar
  66. Scervino JM, Mesa MP, Mo’nica ID, Recchi M, Moreno NS, Godeas A (2010) Soil fungal isolates produce different organic acid patterns involved in phosphate salts solubilization. Biol Fertil Soils 46:755–763CrossRefGoogle Scholar
  67. Shahid M, Hameed S, Imran A, Ali S, Elsas JD (2012) Root colonization and growth promotion of sunflower (Helianthus annuus L.) by phosphate solubilizing Enterobacter sp. Fs-11. World J Microbiol Biotechnol 28(2):749–2758CrossRefGoogle Scholar
  68. Skrary FA, Cameron DC (1998) Purification and characterization of a Bacillus licheniformis phosphatase specific for D-alpha-glycerophosphate. Arch Biochem Biophys 349:27–35CrossRefGoogle Scholar
  69. Sperber JI (1958a) The incidence of apatite-solubilizing organisms in the rhizosphere and soil. Aust J Agric Res 9:778–781CrossRefGoogle Scholar
  70. Sperber JI (1958b) Solubilization of apatite by soil microorganisms producing organic acids. Aust J Agric Res 9:782–787CrossRefGoogle Scholar
  71. Stevenson EJ (1986) Cycles of soil. Wiley, New YorkGoogle Scholar
  72. Taha SM, Mahmoud SAZ, El-Damaty AA, Abd El- Hafez AM (1969) Activity of phosphate dissolving bacteria in Egyptian soil. Plant Soil 31:149CrossRefGoogle Scholar
  73. Thaller MC, Berlutti F, Schippa S, Iori P, Passariello C, Rossolini GM (1995) Heterogeneous patterns of acid phosphatases containing low-molecular-mass Polypeptides in members of the family Enterobacteriaceae. Int J Syst Evol Microbiol 4:255–261Google Scholar
  74. Tilak KVBR, Ranganayaki NL, Pal KK, De R, Saxena AK, Nautiyal CS, Mittal S, Tripathi AK, Johri BN (2005) Diversity of plant growth and soil health supporting bacteria. Curr Sci 89:136Google Scholar
  75. Tirado R, Allsoapp M (2012) Phosphorus in agriculture problems and solutions greenpeace research laboratory. Springer, AmsterdemGoogle Scholar
  76. Toro M (2007) Phosphate solubilizing microorganisms in the rhizosphere of native plants from tropical savannas: an adaptive strategy to acid soils? In: Velazquez C, Rodriguez-Barrueco E (eds) Developments in plant and soil sciences. Springer, Dordrecht, pp 249–252Google Scholar
  77. Torriani-Gorini A (1994) Regulation of phosphate metabolism and transport. In: Torriani A, Gorini EY, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 1–4Google Scholar
  78. Van Schie BJ, Hellingwerf KJ, van Dijken JP, Elferink MGL, van Dijl JM, Kuenen JG, Konigns WN (1987) Energy transduction by electron transfer via a pyrrolo-quinoline quinone-dependent glucose dehydrogenase in Escherichia coli, Pseudomonas putida, and Acinetobacter calcoaceticus (var. lwoffii). J Bacteriol 163:493–499Google Scholar
  79. Vazquez P, Holguin G, Puente M, Lopez-cortes A, Bashan Y (2000) Phosphate solubilizing microorganisms associated with the rhizosphere of mangroves in a semi-arid coastal lagoon. Biol Fertil Soils 30:460–468CrossRefGoogle Scholar
  80. Viveros OM, Jorquera MA, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319Google Scholar
  81. Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol 9:174CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wani PA, Khan MS, Zaidi A (2007) Synergistic effects of the inoculation with nitrogen fixing and phosphate-solubilizing rhizobacteria on the performance of field grown chickpea. J Plant Nutr Soil Sci 170:283–287CrossRefGoogle Scholar
  83. Yadav RS, Tarafdar JC (2003) Phytase and phosphatase producing fungi in arid and semi-arid soils and their efficiency in hydrolyzing different organic P compounds. Soil Biol Biochem 35:1–7CrossRefGoogle Scholar
  84. Yi Y, Huang W, Ge Y (2008) Exo-polysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World J Microbiol Biotechnol 24:1059–1065CrossRefGoogle Scholar
  85. Zaidi A, Khan MS (2005) Interactive effect of rhizospheric microorganisms on growth, yield and nutrient uptake of wheat. J Plant Nutr 28:2079–2092CrossRefGoogle Scholar
  86. Zaidi A, Khan MS, Ahemad M, Oves M (2009a) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Immunol Hung 56:263–284CrossRefPubMedGoogle Scholar
  87. Zaidi A, Khan MS, Ahemad M, Oves M, Wani PA (2009b) Recent advances in plant growth promotion by phosphate-solubilizing microbes. In: Khan MS et al (eds) Microbial strategies for crop improvement. Springer, Berlin/Heidelberg, pp 23–50CrossRefGoogle Scholar
  88. Zhu F, Qu L, Hong X, Sun X (2011) Isolation and characterization of a phosphate solubilizing halophilic bacterium Kushneria sp. YCWA18 from Daqiao Saltern on the coast of Yellow Sea of China. Evid Based Complement Alternat Med:1–6Google Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • A. Pradhan
    • 1
  • A. Pahari
    • 1
  • S. Mohapatra
    • 1
  • Bibhuti Bhusan Mishra
    • 2
    Email author
  1. 1.Department of MicrobiologyCollege of Basic Science & Humanities, Orissa University of Agriculture and TechnologyBhubaneswarIndia
  2. 2.Department of MicrobiologyOrissa University of Agriculture and TechnologyBhubaneswarIndia

Personalised recommendations