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Cold-Adapted and Rhizosphere-Competent Strain of Rahnella sp. with Broad-Spectrum Plant Growth-Promotion Potential

  • Vyas, Pratibha (Plant Pathology and Microbiology Laboratory, Hill Area Tea Science, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research) ;
  • Joshi, Robin (Biochemistry Laboratory, Hill Area Tea Science, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research) ;
  • Sharma, K.C. (Krishi Vigyan Kendra, CSK Himachal Pradesh Krishi Vishvavidyalaya) ;
  • Rahi, Praveen (Plant Pathology and Microbiology Laboratory, Hill Area Tea Science, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research) ;
  • Gulati, Ashu (Biochemistry Laboratory, Hill Area Tea Science, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research) ;
  • Gulati, Arvind (Plant Pathology and Microbiology Laboratory, Hill Area Tea Science, Institute of Himalayan Bioresource Technology, Council of Scientific and Industrial Research)
  • Received : 2010.07.14
  • Accepted : 2010.09.14
  • Published : 2010.12.28

Abstract

A phosphate-solubilizing bacterial strain isolated from Hippophae rhamnoides rhizosphere was identified as Rahnella sp. based on its phenotypic features and 16S rRNA gene sequence. The bacterial strain showed the growth characteristics of a cold-adapted psychrotroph, with the multiple plant growth-promoting traits of inorganic and organic phosphate solubilization, 1-aminocyclopropane-1-carboxylate-deaminase activity, ammonia generation, and siderophore production. The strain also produced indole-3-acetic acid, indole-3-acetaldehyde, indole-3-acetamide, indole-3-acetonitrile, indole-3-lactic acid, and indole-3-pyruvic acid in tryptophan-supplemented nutrient broth. Gluconic, citric and isocitric acids were the major organic acids detected during tricalcium phosphate solubilization. A rifampicin-resistant mutant of the strain exhibited high rhizosphere competence without disturbance to the resident microbial populations in pea rhizosphere. Seed bacterization with a charcoal-based inoculum significantly increased growth in barley, chickpea, pea, and maize under the controlled environment. Microplot testing of the inoculum at two different locations in pea also showed significant increase in growth and yield. The attributes of cold-tolerance, high rhizosphere competence, and broad-spectrum plant growth-promoting activity exhibited the potential of Rahnella sp. BIHB 783 for increasing agriculture productivity.

Keywords

References

  1. Anandham, R., P. Indira Gandhi, M. Madhaiyan, and T. M. Sa. 2008. Potential plant growth promoting traits and bioacidulation of rock phosphate by thiosulfate oxidizing bacteria isolated from crop plants. J. Basic Microbiol. 48: 439-447. https://doi.org/10.1002/jobm.200700380
  2. Bakker, A. W. and B. Schippers. 1987. Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp. mediated plant growth reduction. Soil Biol. Biochem. 19: 452-458.
  3. Behbahani, M. 2010. Investigation of biological behavior and colonization ability of Iranian indigenous phosphate solubilizing bacteria. Scientia Horticult. 124: 393-399. https://doi.org/10.1016/j.scienta.2010.01.019
  4. Bell, C. R., G. A. Dickie, and J. W. Y. F. Chan. 1995. Variable response of bacteria isolated from grapevine xylem to control grape crown gall disease in planta. Am. J. Enol. Vitic. 46: 499-508.
  5. Berge, O., T. Heulin, W. Achouak, C. Richard, R. Bally, and J. Balandreau. 1991. Rahnella aquatilis, a nitrogen-fixing enteric bacterium associated with the rhizosphere of wheat and maize. Can. J. Microbiol. 37: 195-203. https://doi.org/10.1139/m91-030
  6. Cappuccino, J. C. and N. Sherman. 1992. Microbiology: A Laboratory Manual, pp. 125-179. Benjamin/Cummings Pub. Co., New York.
  7. Castric, P. A. 1975. Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can. J. Microbiol. 21: 613-618. https://doi.org/10.1139/m75-088
  8. Chung, K. R., T. Shilts, U. Erturk, L. W. Timmer, and P. P. Uneg. 2003. Indole derivatives produced by the fungus Colletotrichum acutatum causing lime anthracnose and postbloom fruit drop of citrus. FEMS Microbiol. Lett. 226: 23-30. https://doi.org/10.1016/S0378-1097(03)00605-0
  9. Dey, R., K. K. Pal, D. M. Bhatt, and S. M. Chauhan. 2004. Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth promoting rhizobacteria. Microbiol. Res. 159: 371-394. https://doi.org/10.1016/j.micres.2004.08.004
  10. Duponois, R., M. Kisa, and C. Plenchette. 2006. Phosphate solubilizing potential of the nematophagous fungus Arthrobotrys oligospora. J. Plant Nutr. Soil Sci. 169: 280-282. https://doi.org/10.1002/jpln.200520551
  11. Egamberdiyeva, D., D. Juraeva, L. Gafurova, and G. Hoflich. 2002. Promotion of plant growth of maize by plant growth promoting bacteria in different temperatures and soils. In E. van Santen (ed.). Making Conservation Tillage Conventional: Building a Future on 25 Years of Research. Special Report No. 1, Proceedings of the 25th Annual Southern Conservation Tillage Conference for Sustainable Agriculture, Auburn, AL. Alabama Agricultural Experiment and Auburn University, AL 36849, USA.
  12. El-Hendawy, H. H., M. E. Osman, and N. M. Sorour. 2005. Biological control of bacterial spot of tomato caused by Xanthomonas campestris pv. vesicatoria by Rahnella aquatilis. Microbiol. Res. 160: 343-352. https://doi.org/10.1016/j.micres.2005.02.008
  13. Farajzadeh, D., N. Aliasgharzad, N. S. Bashir, and B. Yakhchali. 2010. Cloning and characterization of a plasmid-encoded ACC deaminase from an indigenous Pseudomonas fluorescens FY32. Curr. Microbiol. 61: 37-43. https://doi.org/10.1007/s00284-009-9573-x
  14. Fernandez, L. A., P. Zalba, M. A. Gomez, and M. A. Sagardoy. 2007. Phosphate-solubilization activity of bacterial strains in soil and their effect on soybean growth under greenhouse conditions. Biol. Fert. Soils 43: 805-809. https://doi.org/10.1007/s00374-007-0172-3
  15. Ge, S. M., L. Tao, and S. F. Chen. 2009. Expression and functional analysis of aminotransferase involved in indole-3-acetic acid biosynthesis in Azospirillum brasilense Yu62. Biochemistry 74: 81-84.
  16. Glick, B. R., Z. Cheng, J. Czarny, and J. Duan. 2007. Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur. J. Plant Pathol. 119: 329-339. https://doi.org/10.1007/s10658-007-9162-4
  17. Gulati, A., P. Rahi, and P. Vyas. 2008. Characterization of phosphate-solubilizing fluorescent pseudomonads from rhizosphere of seabuckthorn growing in cold deserts of Himalayas. Curr. Microbiol. 56: 73-79. https://doi.org/10.1007/s00284-007-9042-3
  18. Gulati, A., P. Vyas, P. Rahi, and R. C. Kasana. 2009. Plant growth promoting and rhizosphere competent Acinetobacter rhizosphaerae strain BIHB 723 from the cold deserts of Himalayas. Curr. Microbiol. 58: 371-377. https://doi.org/10.1007/s00284-008-9339-x
  19. Huang, H., H. Luo, Y. Wang, D. Fu, N. Shao, G. Wang, P. Yang, and B. Yao. 2008. A novel phytase from Yersinia rohdei with high phytate hydrolysis activity under low pH and strong pepsin conditions. Appl. Microbiol. Biotechnol. 80: 417-426. https://doi.org/10.1007/s00253-008-1556-5
  20. Idriss, E. E., O. Makarewicz, A. Farouk, K. Rosner, R. Greiner, H. Bochow, T. Richter, and R. Borriss. 2002. Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant growth-promoting effect. Microbiology 148: 2097-2109.
  21. Jacobson, B. C., J. J. Pasternak, and B. R. Glick. 1994. Partial purification and characterization of 1-aminocyclopropane-1-carboxylate deaminase from the plant growth promoting rhizobacterium Pseudomonas putida GR 12-2. Can. J. Microbiol. 40: 1019-1025. https://doi.org/10.1139/m94-162
  22. Jackson, M. L. 1973. Soil Chemical Analysis. Prentice Hall, New Delhi, India.
  23. Johri, J. K., S. Surange, and C. S. Nautiyal. 1999. Occurrence of salt, pH and temperature-tolerant phosphate-solubilizing bacteria in alkaline soils. Curr. Microbiol. 39: 89-93. https://doi.org/10.1007/s002849900424
  24. Khan, A. A., G. Jilani, M. S. Akhtar, S. M. S. Naqvi, and M. Rasheed. 2009. Phosphorus solubilizing bacteria: Occurrence, mechanisms and their role in crop production. J. Agric. Biol. Sci. 1: 48-58.
  25. Kim, K. Y., D. Jordan, and H. B. Krishnan. 1997. Rahnella aquatilis, a bacterium isolated from soybean rhizosphere, can solubilize hydroxyapatite. FEMS Microbiol. Lett. 153: 273-277. https://doi.org/10.1016/S0378-1097(97)00246-2
  26. Krieg, N. R. and J. G. Holt. 1984. Bergey's Manual of Systematic Bacteriology, Vol. 1. Williams and Willkins, Baltimore
  27. Kuklinsky-Sobrat, J., W. L. Araujo, R. Mendes, I. O. Geraldi, A. A. Pizzirani-Kleiner, and J. L. Azevedo. 2004. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol. 6: 1244-1251. https://doi.org/10.1111/j.1462-2920.2004.00658.x
  28. Kumar, K. V., S. Srivastava, N. Singh, and H. M. Behl. 2009. Role of metal resistant plant growth promoting bacteria in ameliorating fly ash to the growth of Brassica juncea. J. Hazard. Mater. 170: 51-57. https://doi.org/10.1016/j.jhazmat.2009.04.132
  29. Lugtenberg, B. J. J., L. Dekkers, and G. V. Bloemberg. 2001. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 39: 461-490. https://doi.org/10.1146/annurev.phyto.39.1.461
  30. Mishra, P. K., S. Mishra, G. Selvakumar, S. C. Bisht, J. K. Bisht, S. Kundu, and H. S. Gupta. 2008. Characterization of a psychrotolerant plant growth promoting Pseudomonas sp. strain PGERs17 (MTCC 9000) isolated from North Western Indian Himalayas. Ann. Microbiol. 58: 561-568. https://doi.org/10.1007/BF03175558
  31. Nautiyal, C. S. 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett. 170: 265-270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
  32. Negi, Y. K., S. K. Garg, and J. Kumar. 2005. Cold tolerant fluorescent Pseudomonas isolates from Garhwal Himalayas as potential plant growth promoting and biocontrol agents in pea. Curr. Sci. 89: 2151-2156.
  33. Park, K. H., C. Y. Lee, and H. J. Son. 2009. Mechanism of insoluble phosphate solubilization by Pseudomonas fluorescens RAF15 isolated from ginseng rhizosphere and its plant growthpromoting activities. Lett. Appl. Microbiol. 49: 222-228. https://doi.org/10.1111/j.1472-765X.2009.02642.x
  34. Patel, D. K., G. Archana, and G. N. Kumar. 2008. Variation in the nature of organic acid secretion and mineral phosphate solubilization by Citrobacter sp. DHRSS in the presence of different sugars. Curr. Microbiol. 56: 168-174. https://doi.org/10.1007/s00284-007-9053-0
  35. Payne, S. M. 1994. Detection, isolation and characterization of siderophores. Methods Enzymol. 235: 329-344. https://doi.org/10.1016/0076-6879(94)35151-1
  36. Penrose, D. M. and B. R. Glick. 2003. Methods for isolating and characterizing ACC deaminase-containing plant growth promoting rhizobacteria. Plant Physiol. 118: 10-15. https://doi.org/10.1034/j.1399-3054.2003.00086.x
  37. Poonguzhali, S., M. Madhaiyan, and T. Sa. 2008. Isolation and identification of phosphate solubilizing bacteria from Chinese cabbage and their effect on growth and phosphorus utilization of plants. J. Microbiol. Biotechnol. 18: 773-777.
  38. Rodriguez, R., R. Fraga, T. Gonzalez, and Y. Bashan. 2006. Genetics of phosphate solubilization and its potential applications for improving plant growth promoting bacteria. Plant Soil 287: 15-21. https://doi.org/10.1007/s11104-006-9056-9
  39. Richardson, A. E. and P. A. Hadobas. 1997. Soil isolates of Pseudomonas spp. that utilize inositol phosphates. Can. J. Microbiol. 43: 509-516. https://doi.org/10.1139/m97-073
  40. Sarwar, M. and J. W. T. Frankenberger. 1994. Tryptophan dependent biosynthesis of auxins in soil. Plant Soil 160: 97-104. https://doi.org/10.1007/BF00150350
  41. Sasser, M. 1990. Tracking a strain using the microbial identification system. Technical Note 102, MIS, Newark, DE.
  42. Schwyn, B. and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 45-56.
  43. Selvakumar, G., M. Mohan, M. S. Kundu, A. D. Gupta, P. Joshi, S. Nazim, and H. S. Gupta. 2008. 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.
  44. Selvakumar, G., S. Kundu, P. Joshi, S. Nazim, A. D. Gupta, P. K. Mishra, and H. S. Gupta. 2008. Characterization of a coldtolerant 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. https://doi.org/10.1007/s11274-007-9558-5
  45. Selvakumar, G., S. Kundu, P. Joshi, A. D. Gupta, and H. S. Gupta. 2009. Growth promotion of wheat seedlings by Exiguobacterium acetylicum 1P (MTCC 8707) a cold tolerant bacterial strain from the Uttarakhand Himalayas. Indian J. Microbiol. 50: 50-56.
  46. Selvakumar, G., P. Joshi, S. Nazim, P. K. Mishra, J. K. Bisht, and H. S. Gupta. 2009. Phosphate solubilization and growth promotion by Pseudomonas fragi CS11RH1 (MTCC 8984), a psychrotolerant bacterium isolated from a high altitude Himalayan rhizosphere. Biologia 64: 239-245. https://doi.org/10.2478/s11756-009-0041-7
  47. Son, H. J., G. T. Park, M. S. Cha, and M. S. Heo. 2006. Solubilization of insoluble inorganic phosphates by a novel salt and pH-tolerant Pantoea agglomerans R-42 isolated from soybean rhizosphere. Biores. Technol. 97: 204-210. https://doi.org/10.1016/j.biortech.2005.02.021
  48. Tsavkelova, E. A., T. A. Cherdyntseva, S. G. Botina, and A. I. Netrusov. 2007. Bacteria associated with orchid roots and microbial production of auxin. Microbiol. Res. 162: 69-76. https://doi.org/10.1016/j.micres.2006.07.014
  49. Vargas, F. R. D. and G. W. O'Hara. 2006. Isolation and characterization of rhizosphere bacteria with potential for biological control of weeds in vineyards. J. Appl. Microbiol. 100: 946-954. https://doi.org/10.1111/j.1365-2672.2006.02851.x
  50. Vyas, P. and A. Gulati. 2009. Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol. 9: 174. https://doi.org/10.1186/1471-2180-9-174
  51. Vyas, P., P. Rahi, and A. Gulati. 2009. Stress tolerance and genetic variability of phosphate-solubilizing fluorescent Pseudomonas from the cold desert of the trans-Himalayas. Microb. Ecol. 58: 425-434. https://doi.org/10.1007/s00248-009-9511-2
  52. Wei, H. L. and L. Q. Zhang. 2006. Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24. Antonie van Leeuwenhoek 89: 267-280. https://doi.org/10.1007/s10482-005-9028-8
  53. Weisburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S Ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173: 697-703.

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