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Volume 64, Issue 2 (Apr 2009)


Phosphate solubilization and growth promotion by Pseudomonas fragi CS11RH1 (MTCC 8984), a psychrotolerant bacterium isolated from a high altitude Himalayan rhizosphere

Govindan Selvakumar / Piyush Joshi / Sehar Nazim / Pankaj Mishra / Jaideep Bisht / Hari Gupta
Published Online: 2009-02-20 | DOI: https://doi.org/10.2478/s11756-009-0041-7


Phosphate solubilization and growth promotion by Pseudomonas fragi CS11RH1 (MTCC 8984), a psychrotolerant bacterium isolated from a high altitude garlic rhizosphere from the Indian Himalayas, are reported here. The identity of the isolate was arrived on the basis of its biochemical features and sequencing of the 16S rRNA gene. The isolate grew and solubilized phosphate at temperatures ranging from 4 to 30°C. Besides solubilizing P it produced indole acetic acid (IAA) and hydrogen cyanide (HCN). Seed bacterization with the isolate significantly increased the percent germination, rate of germination, plant biomass and nutrient uptake of wheat seedlings. While Pseudomonas fragi is normally associated with the spoilage of dairy products stored at cold temperatures, this is an early report on the plant growth promoting ability of the bacterium.

Keywords: psychrotolerant; Pseudomonas fragi; phosphate solubilization; plant growth promotion

  • [1] Ali Z., O’Hare W.T. & Theaker B.J. 2003. Detection of bacterial contaminated milk by means of a quartz crystal microbalance based electronic nose. J. Therm. Anal. Calorim. 71: 155–161. http://dx.doi.org/10.1023/A:1022274419166CrossrefGoogle Scholar

  • [2] Alquati C., De Gioia L., Santarossa G., Alberghina L., Fantucci P. & Lotti M. 2002. The cold-active lipase of Pseudomonas fragi heterologous expression, biochemical characterization and molecular modeling. Eur. J. Biochem. 269: 3321–3328. http://dx.doi.org/10.1046/j.1432-1033.2002.03012.xCrossrefGoogle Scholar

  • [3] Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403–410. CrossrefGoogle Scholar

  • [4] Asea P.E.A., Kucey R.M.N. & Stewart J.W.B. 1988. Inorganic phosphate solubilization by two Penicillium species in solution culture and soil. Soil Biol. Biochem. 20: 459–464. http://dx.doi.org/10.1016/0038-0717(88)90058-2CrossrefGoogle Scholar

  • [5] Atlas R.M. 1995. The Handbook of Microbiological Media for the Examination of Food. CRC Press, Boca Raton, 197 pp. Google Scholar

  • [6] Bakker A.W. & Schipper B. 1987. Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp. mediated plant growth stimulation. Soil Biol. Biochem. 19: 451–457. http://dx.doi.org/10.1016/0038-0717(87)90037-XCrossrefGoogle Scholar

  • [7] Chen Y.P., Rekha P.D., Arun A.B., Shen F.T., Lai W.A. & Young C.C. 2006. Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl. Soil Ecol. 34: 33–41. http://dx.doi.org/10.1016/j.apsoil.2005.12.002CrossrefGoogle Scholar

  • [8] Chung H., Par M., Madhaiyan M., Seshadri S., Song J., Cho H. & Sa T. 2005. Isolation and characterization of phosphate solubilization bacteria from the rhizosphere of crop plant of Korea. Soil Biol. Biochem. 37: 1970–1974. http://dx.doi.org/10.1016/j.soilbio.2005.02.025CrossrefGoogle Scholar

  • [9] Collins C.H. & Lyne P.M. 1980. Microbiological Methods. Butterworth and Co., Ltd., London. Google Scholar

  • [10] Di Simine C.D., Sayer J.A. & Gadd G.M. 1998. Solubilization of zinc phosphate by a strain of Pseudomonas fluorescens isolated from a forest soil. Biol. Fertil. Soils 28: 87–94. http://dx.doi.org/10.1007/s003740050467CrossrefGoogle Scholar

  • [11] Elliot L.F. & Lynch J.M. 1984. Pseudomonas as a factor in the growth of winter wheat (Triticum aestivum L.). Soil Biol. Biochem 16: 69–71. http://dx.doi.org/10.1016/0038-0717(84)90128-7CrossrefGoogle Scholar

  • [12] Fernandez L.A., Zalba P., Gomez M.A. & Sagardoy M.A. 2007. Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol. Fertil. Soils 43: 805–809. http://dx.doi.org/10.1007/s00374-007-0172-3CrossrefGoogle Scholar

  • [13] Gaind S. & Gaur A.C. 1991. Thermotolerent phosphate solubilizing microorganisms and their interaction with mung-bean. Plant Soil 133: 141–149. http://dx.doi.org/10.1007/BF00011908CrossrefGoogle Scholar

  • [14] Goldstein A. 1995. Recent progress in understanding the molecular genetics and biochemistry of calcium phosphate solubilization by Gram negative bacteria. Biol. Agric. Hortic. 12: 185–193. CrossrefGoogle Scholar

  • [15] Gordon A.S. & Weber R.P. 1951. Colorimetric estimation of indole acetic acid. Plant Physiol. 26: 192–195. http://dx.doi.org/10.1104/pp.26.1.192CrossrefGoogle Scholar

  • [16] Gulati A., Rahi P. & Vyas P. 2008. Characterization of phosphate-solubilizing fluorescent Pseudomonads from the rhizosphere of seabuckthorn growing in the cold deserts of Himalayas. Curr. Microbiol. 56: 73–79. http://dx.doi.org/10.1007/s00284-007-9042-3CrossrefGoogle Scholar

  • [17] Hameeda B., Rupela O.P. & Reddy G. 2006. Application of plant growth-promoting bacteria associated with composts and macrofauna for growth promotion of pearl millet (Pennisetum glaucum L.). Biol. Fertil. Soils 43: 221–227. http://dx.doi.org/10.1007/s00374-006-0098-1CrossrefGoogle Scholar

  • [18] Holland M.A. 1997. Occams razor applied to hormonology. Are cytokinins produced by plants? Plant Physiol. 115: 865–868. Google Scholar

  • [19] Hosseini S.Z. & Jafari M. 2002. Investigation on effect of salinity stress on germination of three accessions of tall wheat grass (Agropyron elongatum). Paper No. 2289, 17th World Congress on Soil Science, 14–21 August 2002, Thailand. Google Scholar

  • [20] Hwangbo H., Park R.D., Kim Y.W., Rim Y.S., Park K.H., Kim T.H., Suh J.S. & Kim K.Y. 2003. 2-Ketogluconic acid production and phosphate solubilization by Enterobacter intermedium. Curr. Microbiol. 47: 87–92. http://dx.doi.org/10.1007/s00284-002-3951-yGoogle Scholar

  • [21] Jackson M.L. 1973. Soil Chemical Analysis. Prentice Hall, Ltd., New Delhi. Google Scholar

  • [22] Jones D.L. & Darrah P.R. 1994. Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166: 247–257. http://dx.doi.org/10.1007/BF00008338CrossrefGoogle Scholar

  • [23] Katiyar V. & Goel R. 2003. Solubilization of inorganic phosphate and plant growth promotion by cold tolerant mutants of Pseudomonas fluorescens. Microbiol. Res. 158: 163–168. http://dx.doi.org/10.1078/0944-5013-00188CrossrefGoogle Scholar

  • [24] Khalid A., Arshad M. & Zahir Z.A. 2004. Screening plant growth promoting rhizobacteria for improving growth and yield of wheat. J. Appl. Microbiol. 96: 473–480. http://dx.doi.org/10.1046/j.1365-2672.2003.02161.xCrossrefGoogle Scholar

  • [25] Kim K.Y., Hwangbo H, Kim Y.W., Kim H.J., Park K.H., Kim Y.C. & Seoung K.Y. 2002.Organic acid production and phosphate solubilization by Enterobacter intermedium 60-2G. Korean J. Soil Sci. Fert. 35: 59–67. Google Scholar

  • [26] Kimura M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120. http://dx.doi.org/10.1007/BF01731581CrossrefGoogle Scholar

  • [27] Kloepper J.W., McInroy J.A. & Bowen K.L. 1992. Comparative identification by fatty acid analysis of soil, rhizosphere and geocarposphere bacteria of peanut (Arachis hypogaea L.). Plant Soil 139: 85–90. http://dx.doi.org/10.1007/BF00012845CrossrefGoogle Scholar

  • [28] Kremer R.J. & Souissi T. 2001. Cyanide production by rhizobacteria and potential for suppression of wheat seedling growth. Curr. Microbiol. 43: 182–186. http://dx.doi.org/10.1007/s002840010284CrossrefGoogle Scholar

  • [29] Kumar S., Tamura K. & Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5: 150–163. http://dx.doi.org/10.1093/bib/5.2.150CrossrefGoogle Scholar

  • [30] Lambers H. 1982. Cyanide-resistant respiration: a non phosphorylating electron transport pathway acts as an energy over-flow. Physiol. Plant 55: 478–485. http://dx.doi.org/10.1111/j.1399-3054.1982.tb04530.xCrossrefGoogle Scholar

  • [31] Lebert I., Begot C. & Lebert A. 1998. Growth of Pseudomonas fluorescens and Pseudomonas fragi in a meat medium as affected by pH (5.8–7.0), water activity (0.97–1.00) and temperature (7–25 °C). Int. J. Food Microbiol. 39: 53–60. http://dx.doi.org/10.1016/S0168-1605(97)00116-5Google Scholar

  • [32] Lifshitz R., Kloepper J.W., Kozlowski M., Simonson C., Carlson J., Tipping E.N. & Zaleska I. 1987. Growth promotion of canola (rape-seed) seedlings by a strain of Peudomonas putida under gnotobiotic conditions. Can. J. Microbiol. 8: 102–106. Google Scholar

  • [33] Martin L., Velazquez E., Rivas R., Mateos P.F., Martinez-Molina E., Rodriguez-Barrueco C. & Peix A. 2003. Effect of inoculation with a strain of Pseudomonas fragi on the growth and phosphorus content of strawberry plants, pp. 309–315. In: Velazquez E. & Rodriguez-Barrueco C. (eds), First International Meeting on Microbial Phosphate Solubilization (19–22 July 2002, Salamanca, Spain), Springer, The Netherlands. Google Scholar

  • [34] Mehta S. & Nautiyal C.S. 2001. An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr. Microbiol. 43: 51–56. http://dx.doi.org/10.1007/s002840010259CrossrefGoogle Scholar

  • [35] Murphy J.P. & Riley J.P. 1962. A modified single solution method for the determination of the phosphate in natural waters. Anal. Chim. Acta 27: 31–36. http://dx.doi.org/10.1016/S0003-2670(00)88444-5CrossrefGoogle Scholar

  • [36] Musarrat J., Bano N. & Rao R.A.K. 2000. Isolation and characterization of 2,4-dichlorophenoxyacetic acid-catabolizing bacteria and their biodegradation efficiency in soil. World J. Microbiol. Biotechnol. 16: 495–497. http://dx.doi.org/10.1023/A:1008945720327CrossrefGoogle Scholar

  • [37] Nakeeran S., Fernando W.G.D. & Siddiqui Z.A. 2005. Plant growth promoting rhizobacteria formulations and its scope in commercialization for the management of pests and diseases, pp. 257–296. In: Siddiqui Z.A. (ed.), PGPR Biocontrol and Biofertilization, Springer. Google Scholar

  • [38] Oehl F., Oberson A., Probst M., Fliessbach A., Roth H.R. & Frossard E. 2001. Kinetics of microbial phosphorus uptake in cultivated soils. Biol. Fertil. Soil 34: 31–41. http://dx.doi.org/10.1007/s003740100362CrossrefGoogle Scholar

  • [39] Olsen S.R. & Sommers L.E. 1982. Phosphorus, pp. 403–430. In: Page A.L., Miller A.L. & Keeney R.H. (eds), Methods of Soil Analysis, part 2, Chemical and Microbiological Properties. American Society of Agronomy, Madison, Wisconsin, USA. Google Scholar

  • [40] Pal S.S. 1998. Interaction of an acid tolerant strain of phosphate solubilizing bacteria with a few acid tolerant crops. Plant Soil 198: 169–177. http://dx.doi.org/10.1023/A:1004318814385CrossrefGoogle Scholar

  • [41] Pandey A. & Palni L.M.S. 1998. Isolation of Pseudomonas corrugata from Sikkim Himalayas. World J. Microbiol. Biotechnol. 14: 411–413. http://dx.doi.org/10.1023/A:1008825514148CrossrefGoogle Scholar

  • [42] Pandey A., Trivedi P., Kumar B. & Palni L.M.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: 102–107. http://dx.doi.org/10.1007/s00284-006-4590-5Google Scholar

  • [43] Peix A., Rivas R., Mateos P.F., Martinez-Molina E., Rodrigue Barrueco C. & Velazquez E. 2003. Pseudomonas rhizosphaerae sp. nov., a novel species that actively solubilizes phosphate in vitro. Int. J. Syst. Evol. Microbiol. 53: 2067–2072. http://dx.doi.org/10.1099/ijs.0.02703-0CrossrefGoogle Scholar

  • [44] Peix A., Rivas R., Santa-Regina I., Mateos P.F., Martinez-Molina E., Rodrigue Barrueco C. & Velazquez E. 2004. Pseudomonas lutea sp. nov., a novel phosphate-solubilizing bacterium isolated from the rhizosphere of grasses. Int. J. Syst. Evol. Microbiol. 54: 847–850. http://dx.doi.org/10.1099/ijs.0.02966-0CrossrefGoogle Scholar

  • [45] Saitou N. & Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425. Google Scholar

  • [46] Sarniguet A., Lucas P., Lucas M. & Samson R. 1992. Soil conduciveness to take all of wheat: influence of the nitrogen fertilizers on the structure of populations of fluorescent pseudomonads. Plant Soil 145: 29–36. http://dx.doi.org/10.1007/BF00009538CrossrefGoogle Scholar

  • [47] Selvakumar G., Kundu S., Joshi P., Nazim S., Gupta A.D., Mishra P.K. & Gupta H.S. 2008. Characterization of a cold-tolerant plant growth-promoting bacterium Pantoea dispersa 1A isolated from a sub-alpine soil in the North Western Indian Himalayas. World J. Microbiol. Biotechnol. 24: 955–960. http://dx.doi.org/10.1007/s11274-007-9558-5Google Scholar

  • [48] Selvakumar G., Mohan M., Kundu S., Gupta A.D., Joshi P., Nazim S. & Gupta H.S. 2007. Cold tolerance and plant growth promotion potential of Serratia marcescens strain SRM (MTCC 8708) isolated from flowers of summer squash (Cucurbita pepo). Lett. Appl. Microbiol. 46: 171–175. http://dx.doi.org/10.1111/j.1472-765X.2007.02282.xCrossrefGoogle Scholar

  • [49] Shivaji S., Chaturvedi P., Reddy G.S.N. & Suresh K. 2005. Pedobacter himalayensis sp. nov., from Hamta glacier located in the Himalayan mountain range in India. Int. J. Syst. Evol. Microbiol. 55: 1083–1088. http://dx.doi.org/10.1099/ijs.0.63532-0CrossrefGoogle Scholar

  • [50] Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. & Higgins D.G. 1997. The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24: 4876–4882. http://dx.doi.org/10.1093/nar/25.24.4876CrossrefGoogle Scholar

  • [51] Trivedi P. & Sa T. 2008. Pseudomonas corrugata (NRRL B-30409) mutants increased phosphate solubilization, organic acid production, and plant growth at low temperatures. Curr. Microbiol. 56: 140–144. http://dx.doi.org/10.1007/s00284-007-9058-8CrossrefGoogle Scholar

  • [52] Vazquez P., Holguin G., Puente M.E., Lopez-Cortez A. & Bashan Y. 2000. Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid costal lagoon. Biol. Fertil. Soil 30: 460–468. http://dx.doi.org/10.1007/s003740050024CrossrefGoogle Scholar

  • [53] Vega N.W.O. 2007. A review on beneficial effects of rhizosphere bacteria on soil nutrient availability and plant nutrient uptake. Revista Facultad Nacional de Agronomia, Medellin 60: 3621–3643. Google Scholar

  • [54] Vessey J.K. 2004. Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255: 571–586. http://dx.doi.org/10.1023/A:1026037216893CrossrefGoogle Scholar

  • [55] Weller D.M. 2002. Microbial population responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40: 309–348. http://dx.doi.org/10.1146/annurev.phyto.40.030402.110010CrossrefGoogle Scholar

About the article

Published Online: 2009-02-20

Published in Print: 2009-04-01

Citation Information: Biologia, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.2478/s11756-009-0041-7.

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