Applied Microbiology and Biotechnology

, Volume 95, Issue 4, pp 851–859 | Cite as

Stress-tolerant P-solubilizing microorganisms

  • N. Vassilev
  • B. Eichler-Löbermann
  • M. Vassileva


Drought, high/low temperature, and salinity are abiotic stress factors accepted as the main reason for crop yield losses in a world with growing population and food price increases. Additional problems create nutrient limitations and particularly low P soil status. The problem of phosphate fertilizers, P plant nutrition, and existing phosphate bearing resources can also be related to the scarcity of rock phosphate. The modern agricultural systems are highly dependent on the existing fertilizer industry based exclusively of this natural, finite, non-renewable resource. Biotechnology offers a number of sustainable solutions that can mitigate these problems by using plant beneficial, including P-solubilizing, microorganisms. This short review paper summarizes the current and future trends in isolation, development, and application of P-solubilizing microorganisms in stress environmental conditions bearing also in mind the imbalanced cycling and unsustainable management of P. Special attention is devoted to the efforts on development of biotechnological strategies for formulation of P-solubilizing microorganisms in order to increase their protection against adverse abiotic factors.


Abiotic stress factors Microbial P-solubilization Stress tolerance Inoculant formulation 



This work was supported by Projects CTM2008-03524, CTM2011-027797 (Ministerio de Ciencia e Innovación, España), P09-RNM-5196 (Project from the Junta de Andalucía, Proyecto de Excelencia), and EU COST FA0905 and FA1103. NV is grateful for the SABF PR2010-0422—Ministerio de Educacion, España and DAAD-Germany.


  1. Ali H, Tucher TC, Thompson TL, Salim M (2001) Effects of salinity and mixed ammonium and nitrate nutrition on the growth and nitrogen utilization of barley. J Agron Crop Sci 186:223–228CrossRefGoogle Scholar
  2. Arora NK, Khare E, Maheshwari DK (2011) Plant growth promoting rhizobacteria: Constraints in bioformulation, commercialization, and future strategies. In Maheshwari DK (ed) Plant growth and health promoting bacteria. Microbiology Monographs vol. 18. Springer, pp. 97–116.Google Scholar
  3. Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirilum sp. under drought stress. World J Microbiol Biotechnol 27:197–205CrossRefGoogle Scholar
  4. Banerjee S, Palit R, Sengupta Ch, Standing D (2010) Stress induces phosphate solubilisation by Arthrobacter sp. and Bacillus sp. isolated from tomato rhizosphere. Aust J Crop Sci 4:378–383Google Scholar
  5. Barrow JR, Osuna P (2002) Phosphorus solubilization and uptake by dark septate fungi in fourwing saltbush, Atriplex canescens (Pursh) Nutt. J Arid Environ 51:449–459CrossRefGoogle Scholar
  6. Barrow JR, Osuna-Avila P, Reyes-Vera I (2004) Fungal endophytes intrinsincally associated with micropropagated plants regenerated from native Bouteloua eriopoda Torr and Atroplex canescens (Pursh) Nutt. In Vitro Cell Dev Biol Plant 40:608–612CrossRefGoogle Scholar
  7. Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 15:729–770CrossRefGoogle Scholar
  8. Berbee ML (2001) The phylogeny of plant and animal pathogens in the Ascomycota. Physiol Mol Plant Pathol 59:165–187CrossRefGoogle Scholar
  9. Blackwell M (2000) Terrestrial life-fungal from the start? Science 289:1884–1885CrossRefGoogle Scholar
  10. Chaiharn M, Lumyong S (2009) Phosphate solubilisation potential and stress tolerance of rhizobacteria from rice soil in Northern Thailand. World J Microbiol Biotechnol 25:305–314CrossRefGoogle Scholar
  11. Chanway CP, Hall FB (1994) Growth of out planted lodepole pine seedlings one year after inoculation with plant growth promoting rhizobacteria. Forest Sci 40:238–246Google Scholar
  12. Consensus Statement Declaration (2011) Sustainable phosphorus summit, Tempe, Arizona, USA, ASU School of Life SciencesGoogle Scholar
  13. Das K, Katiyar V, Goel R (2003) P solubilisation potential of plant growth promoting Pseudomonas mutants at low temperature. Microbiol Res 158:359–362CrossRefGoogle Scholar
  14. Dey C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(1682):1694Google Scholar
  15. Egamberdieva D, Kucharova Z (2009) Selection for root colonising bacteria stimulating wheat growth in saline soils. Biol Fertil Soils 45:563–571CrossRefGoogle Scholar
  16. Egamberdiyeva D, Höflich G (2003) Influence of growth-promoting on the growth of wheat in different soils and temperatures. Soil Biol Biochem 35:973–978CrossRefGoogle Scholar
  17. FAO (2005) Global network on integrated soil management for sustainable use of salt-affected soils. FAO. Land and Plant Nutrition Management Service, RomeGoogle Scholar
  18. Gaind S, Gaur A (1991) Thermotolerant phosphate solubilizing microorganisms and their interaction with mungbean. Plant Soil 133:141–149CrossRefGoogle Scholar
  19. Goldstein AH, Rogers RD (1999) Biomediated continuous release phosphate fertilizer. US Patent 5:912,398Google Scholar
  20. Grover M, Ali Sk Z, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agricultural crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240CrossRefGoogle Scholar
  21. Gulati A, Rahi P, Vyas P (2008) Characterization of phosphate-solubilizing fluorescent Pseudomonas from the rhizosphere of Seabuckthorn growing in the cold deserts of Himalayas. Curr Microbiol 56:73–79CrossRefGoogle Scholar
  22. Gulati A, Vyas P, Rahi P, Kasana RCh (2009) Plant growth-promoting and rhizosphere-competent Acinetobacter rhizosphaerae strain BIHB 723 from the cold deserts of the Himalayas. Curr Microbiol 58:371–377CrossRefGoogle Scholar
  23. Gutierrez-Correa M, Ludeña Y, Ramage G, Villena GK (2012) Recent advances on filamentous fungal biofilms for industrial uses. Appl Biochem Biotechnol. doi: 10.1007/s12010-012-9555-5, in press
  24. Haynes RJ, Swift RS (1990) Stability of soil aggregates in relation to organic constituents and soil water content. J Soil Sci 41:73–83CrossRefGoogle Scholar
  25. Holker U, Lenz J (2005) Solid-state fermentation—are there any biotechnological advantages. Curr Opin Microbiol 8:301–306CrossRefGoogle Scholar
  26. Hueso S, Hernandez T, Garcia C (2011) Resistance and resilience of the soil microbial biomass to severe drought in semiarid soils: the importance of organic amendments. Appl Soil Ecol 50:27–36Google Scholar
  27. Ijdo M, Cranenbrouck S, Declerck S (2011) Methods for large-scale production of AM fungi: past, present, and future. Mycorrhiza 21:1–16CrossRefGoogle Scholar
  28. Insam H, Parkinson D, Domsch KH (1989) Influence of macroclimate on soil microbial biomass. Soil Biol Biochem 21:211–221CrossRefGoogle Scholar
  29. Ivanova E, Teunou E, Poncelet D (2005) Allginate based macrocapsules as inoculants carriers for production of nitrogen biofertilizers. Proceedings of the Balkan Scientific Conference of Biology, Plvdiv, Bulgaria (Eds. B Gruev, M Nikolova, A Donev), pp 90–108.Google Scholar
  30. Iyamuremye F, Dick RP (1996) Organic amendments and phosphorus sorption by soils. Adv Agron 56:139–185CrossRefGoogle Scholar
  31. Johri JK, Surange S, Nautiyal CS (1999) Occurrence of salt, pH, and temperature-tolerant, phosphate-solubilizing bacteria in alkaline soils. Curr Microbiol 39:89–93CrossRefGoogle Scholar
  32. Kern J, Hellenbrand HJ, Gömmel M, Ammon Ch, Berg W (2011) Effects of climate factors and soil management on the methane flux in soils from annual and perennial energy crops. Biol Fertil Soils. doi: 10.1007/s00374-011-0603-s
  33. Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable agriculture—a review. Agron Sustain Dev 27:29–43CrossRefGoogle Scholar
  34. Kütük C, Cayci G, Baran A, Baskan O, Hartmann R (2003) Effects of beer factory sludge on soil properties and growth of sugar beet (Beta vulgaris saccharifera L.). Bioresour Technol 90:75–80CrossRefGoogle Scholar
  35. Malusa E, Sas-Paszt K, Ciesielska J (2012) Technologies for beneficial microorganisms as biofertilizers. Sci World J. doi: 10.1100/2012/491206
  36. Maybank J, Bonsal B, Jones K, Lawford R, O’Brien EG, Ripley EA, Wheaton E (1995) Drought as a natural disaster. Atmos Ocean 33:195–222CrossRefGoogle Scholar
  37. Mitchell DA, Berovic M, Krieger N (2002) Overview of solid state bioprocessing. Biotechnol Annu Rev 8:183–225CrossRefGoogle Scholar
  38. Morita RY (1975) Psychrophilic bacteria. Bacteriol Rev 39:144–167Google Scholar
  39. Nautiyal XS, Bhadauria S, Kumar P, Lal K, Mondal R, Verma D (2000) Stress induced phosphate solubilisation in bacteria isolated from alkaline soils. FEMS Microbiol Lett 182:291–296CrossRefGoogle Scholar
  40. Neset T-S, Cordell D (2012) Global phosphorus scarcity: identifying synergies for a sustainable future. J Sci Food Agric 92:2–6CrossRefGoogle Scholar
  41. Pandey A, Trivedi P, Kumar B, Palni Lok Man S (2006) Characterization of a phosphate solubilizing and antagonistic strain of Pseudomonas putida (B0) isolated from a sub-alpine location in the Indian Central Himalaya. Curr Microbiol 53:102–107CrossRefGoogle Scholar
  42. Pascual I, Antolin MC, Garcia C, Polo A, Sanchez-Diaz M (2007) Effect of water deficit on microbial characteristics in soil amended with water sewage sludge or inorganic fertilizer under laboratory conditions. Bioresour Technol 98:29–37CrossRefGoogle Scholar
  43. Rinu K, Pandey A (2011) Slow and steady phosphate solubilisation by a psychrotolerant strain of Paecilomyces hepiali (MTCC 9621). World J Microbiol Biotechnol 27:1055–1062CrossRefGoogle Scholar
  44. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339CrossRefGoogle Scholar
  45. Sandhya V, Ali Sk Z, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by exopolysaccharides producing Pseudomonas putida strain P45. Biol Fertil Sol 46:17–26CrossRefGoogle Scholar
  46. Sandhya V, Ali Sk Z, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62:21–30CrossRefGoogle Scholar
  47. Sardans J, Penuelas J (2005) Drought decreases soil enzyme actiyity in a Mediterranean holm oak forest. Soil Biol Biochem 37:455–461CrossRefGoogle Scholar
  48. Sardans J, Penuelas J, Estiarte M (2006) Warming and drought alter soil phosphatase activity and soil P availability in a Mediterranean shrubland. Plant Soil 289:227–238CrossRefGoogle Scholar
  49. Schulthess FM, Faeth SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia 90:569–578CrossRefGoogle Scholar
  50. Sidari M, Mallamaci C, Muscolo A (2008) Drought, salinity and heat differently affect seed germination of Pinus pinea. J For Res 13:326–330CrossRefGoogle Scholar
  51. Singh SM, Yadav LS, Singh SK, Singh P, Singh PN, Ravindra R (2011) Phosphate solubilizing ability of two Arctic Aspergillus strains. Polar Res 30:7283–7289Google Scholar
  52. Sinsabaugh RC, Antibus RK, Linkins AE, McClaugherty CA, Rayburn L, Repert D, Weiland T (1993) Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:1586–1593CrossRefGoogle Scholar
  53. Soltani A, Gholipoor M, Zeinali E (2006) Seed reserve utilization and seedling growth of wheat as affected by drought and salinity. Environ Exp Bot 55:195–200CrossRefGoogle Scholar
  54. Srividya S, Soumya S, Pooja K (2009) Influence of environmental factors and salinity on phosphate solubilisation by a newly isolated Aspergillus niger F7 from agricultural soil. Afr J Biotechnol 8:1864–1870Google Scholar
  55. Tengerby RP, Szakacs G (2003) Bioconversion of lignocellulose in solid substrate fermentation. Biochem Eng J 13:169–179CrossRefGoogle Scholar
  56. Trivedi P, Sa T (2008) Pseudomonas corrugate (NRRL B-30409) mutants increased phosphate solubilisation, organic acid production, and plant growth at lower temperatures. Curr Microbiol 56:140–144CrossRefGoogle Scholar
  57. Uvarov AV, Tiunov AV, Scheu S (2011) Effects of seasonal and diurnal temperature fluctuations on population dynamics of two epigeic earthworm species in forest soil. Soil Biol Biochem 43:559–570CrossRefGoogle Scholar
  58. Vassilev N, Vassileva M (1992) Production of organic acids by immobilized filamentous fungi. Mycol Res 96:563–570CrossRefGoogle Scholar
  59. Vassilev N, Vassileva M (2003) Biotechnological solubilization of rock phosphate on media containing agro-industrial wastes. Appl Microbiol Biotechnol 61:435–440Google Scholar
  60. Vassilev N, Vassileva M (2005) Gel-entrapment of arbuscular mycorrhizal fungi: Current status and future prospects. Rev Environ Sci Bio/Technol 4:235–243CrossRefGoogle Scholar
  61. Vassilev N, Vassileva M, Fenice M, Federici F (2001a) Immobilized cell technology applied in solubilization of insoluble inorganic (rock) phosphates and P plant acquisition. Bioresour Technol 79:263–271CrossRefGoogle Scholar
  62. Vassilev N, Vassileva M, Azcon R, Medina A (2001b) Application of free and Ca-alginate-entrapped Glomus deserticola and Yarrowia lipolytica in a soil–plant system. J Biotechnol 91:237–242CrossRefGoogle Scholar
  63. Vassilev N, Vassileva M, Azcon R, Medina A (2001c) Interactions of an arbuscular mycorrhizal fungus with free and co-encapsulated cells of Rhizobium trifoli and Yarrowia lipolytica inoculated into a soil-plant system. Biotechnol Lett 23:149–151CrossRefGoogle Scholar
  64. Vassilev N, Vassileva M, Azcon R, Medina A (2001d) Preparation of gel-entrapped mycorrhizal inoculum in the presence or absence of Yarrowia lipolytica. Biotechnol Lett 23:907–909CrossRefGoogle Scholar
  65. Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144CrossRefGoogle Scholar
  66. Vassilev N, Nikolaeva I, Vassileva M (2007a) Indole-3-acetic acid production by gel-entrapped Bacillus thuringiensis in the presence of rock phosphate ore. Chem Eng Commun 194:441–445CrossRefGoogle Scholar
  67. Vassilev N, Vassileva M, Bravo V, Fernandez-Serrano M, Nikolaeva I (2007b) Simultaneous phytase production and rock phosphate solubilisation by Aspergillus niger grown on dry olive wastes. Ind Crop Prod 26:332–336CrossRefGoogle Scholar
  68. Vassilev N, Nikolaeva I, Jurado E, Reyes A, Fenice M, Vassileva M (2008) Antagonistic effect of microbially-treated mixture of agro-industrial wastes and inorganic insoluble phosphate to Fusarium wilt disease. In: Kim Myung-Bo (ed) Progress in environmental microbiology. Nova, USA, pp 223–234Google Scholar
  69. Vassilev N, Someus E, Serrano M, Bravo V, Garcia Roman M, Reyes A, Vassileva M (2009a) Novel approaches in phosphate-fertilizer production based on wastes derived from rock phosphate mining and food processing industry. In: Samuelson JP (ed) Industrial waste: environmental impact, disposal and treatment. Nova, USA, pp 387–391Google Scholar
  70. Vassilev N, Requena A, Nieto L, Nikolaeva I, Vassileva M (2009b) Production of manganese peroxidase by Phanerochaete chrysosporium grown on medium containing agro-wastes/rock phosphate and biocontrol properties of the final product. Ind Crop Prod 30:28–32CrossRefGoogle Scholar
  71. Vassilev N, Reyes A, Altmajer D, Serrano M, Sanchez D, Vassileva M (2010) Ecological effects of microbially-treated hydroxyapatite. 10th International Multidisciplinary Scientific GeoConference. SGEM 2:521–528Google Scholar
  72. Vassileva M, Azcon R, Barea JM, Vassileva N (1999) Effect of encapsulated cells of Enterobacter sp on plant growth and phosphate uptake. Bioresour Technol 67:229–232CrossRefGoogle Scholar
  73. Vassileva M, Azcon R, Barea JM, Vassilev N (2000) Rock phosphate solubilization by free and encapsulated cells of Yarowia lipolytica. Process Biochem 35:693–697CrossRefGoogle Scholar
  74. Vassileva M, Serrano M, Bravo V, Jurado E, Nikolaeva I, Martos V, Vassilev N (2010) Multifunctional properties of phosphate-solubilizing microorganisms grown on agro-industrial wastes in fermentation and soil conditions. Appl Microbiol Biotechnol. doi: 10.1007/s00253-009-2366-0
  75. Vassileva M, Eichler-Löbermann B, Reyes A, Vassilev N (2012) Animal bones char solubilization by gel-entrapped Yarrowia lipolytica on glycerol-based media. Sci World J. doi: 10.1100/2012/907143
  76. Vilchez S, Manzanera M (2011) Biotechnological uses of desiccation-tolerant microorganisms for the rhizoremediation of soils subjected to seasonal drought. Appl Microbiol Biotechnol 91:1297–1304CrossRefGoogle Scholar
  77. Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151CrossRefGoogle Scholar
  78. Wu CH, Bernard SM, Andersen GL, Chen W (2009) Developing microbe–plant interactions for applications in plant-growth promotion and disease control, production of useful compounds, remediation and carbon sequestration. Microb Biotechnol 2:428–440CrossRefGoogle Scholar
  79. Xiao C, Chi R, Li X, Xia M, Xia Z (2011) Biosolubilization of rock phosphate by three stress-tolerant fungal strains. Appl Biochem Biotechnol 165:719–727CrossRefGoogle Scholar
  80. Yadav J, Verma JP, Yadav SK, Tiwari KN (2011) Effect of salt concentration and pH on soil inhabiting fungus Penicillium citrinum Thom. for solubilization of tricalcium phosphate. Microbiol J 1:25–32CrossRefGoogle Scholar
  81. Yang J, Kloepper JW, Ryu C-M (2008) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4CrossRefGoogle Scholar
  82. Yang CH, Chai Q, Huang GB (2010) Root distribution and yield responses of wheat/maize intercropping to alternate irrigation in the arid areas of northwest China. Plant Soil Environ 56:253–262Google Scholar
  83. Yvas P, Rahi P, Chauhan A, Gulati A (2007) Phosphate solubilisation potential and stress tolerance of Eupenicillium parvum from tea soil. Mycol Res 111:931–938CrossRefGoogle Scholar
  84. Zarabi M, Alahdadi I, Akbari GA, Akbari GA (2011) A study on the effects of different biofertilizer combinations on yield, its components and growth indices of corn (Zea mays) under drought stress condition. Afr J Agric Res 6:681–685Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • N. Vassilev
    • 1
    • 2
  • B. Eichler-Löbermann
    • 3
  • M. Vassileva
    • 1
  1. 1.Department of Chemical EngineeringUniversity of GranadaGranadaSpain
  2. 2.Institute of BiotechnologyUniversity of GranadaGranadaSpain
  3. 3.Department of Crop ScienceUniversity of RostockRostockGermany

Personalised recommendations