Effect of phosphorus solubilizing bacteria on some soil properties, wheat yield and nutrient contents

Abstract

Application of chemical fertilizers besides economic concerns has been a reason of environmental and ecosystem degradation, so sustainable organic agriculture is becoming popular in researches and among farming communities. Phosphorus holds second position after nitrogen among macronutrients required for better plant growth and is needed in higher amounts. Meeting this high phosphorus input for better crop yields causes environmental problems like eutrophication, so phosphorus solubilizing bacteria (PSB) and plant growth promoting rhizobacteria (PGPR) are being emphasized to utilize phosphorus fixed in soil layers. This study was carried out to evaluate the effect of PSB on plant growth, soil biological properties including enzymes and soil respiration. Treatments including control, 50 mg kg^-1 nitrogen, 50 mg kg^-1 nitrogen and 12 mg kg^-1 phosphorus applications reduced dosage of nitrogen 25 mg kg^-1 with PGPR and 25 mg kg^-1 nitrogen along with 0.12 g raw phosphate and PGPR. Results indicated that plant parameters like above and below ground plant biomasses (fresh and dry weight), plant nitrogen and phosphorus content were significantly enhanced in all the treatments when compared with the control. While soil pH in rhizosphere significantly increased with the treatments, bulk soil pH decreased with PGPR treatments when compared with all other treatments. EC values in rhizosphere and bulk soils were not significantly influenced with the treatments. Rhizospheric and bulk soil showed high amount of N, P and organic matter in PGPR treatments. Alkaline phosphatase and β-glucosidase activities were found significantly higher in the last treatment than the other treatments. Basal soil respiration was interestingly found higher in control soil but did not differ statistically from the other treatments. Concluding, application of PGPR with lower amounts of chemical fertilizers can reduce the use of chemical fertilizers and has also potential of improving soil health in long term aspects.

Keywords

• Phosphorus solubilizing bacteria,rhizosphere,bulk soil,alkaline phosphatase,β-glucosidase,basal soil respiration

References

1. Abd‐Alla, M.H., 1994. Phosphatases and the utilization of organic phosphorus by Rhizobium leguminosarum biovar viceae. Letters in Applied Microbiology 18(5): 294-296.
2. Afsal, A., Bano, A., 2008. Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum). International Journal of Agriculture and Biology 10(1): 85–88.
3. Akça, M.O., Namlı, A., 2015. Effects of poultry litter biochar on soil enzyme activities and tomato, pepper and lettuce plants growth. Eurasian Journal of Soil Science 4(3): 161-168.
4. Ananyeva, N.D., Rogovaya, S.V., Ivashchenko, K.V., Vasenev, V.I., Sarzhanov, D.A., Ryzhkov, О.V., Kudeyarov, V.N., 2016. Carbon dioxide emission and soil microbial respiration activity of Chernozems under anthropogenic transformation of terrestrial ecosystems. Eurasian Journal of Soil Science 5(2): 146 - 154.
5. Aşkın, T., Kızılkaya, R., 2006. Assessing spatial variability of soil enzyme activities in pasture topsoils using geostatistics. European Journal of Soil Biology 42(4): 230-237.
6. Bartholdy, B.A., Berreck, M., Haselwandter, K., 2001. Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biometals 14(1):33-42.
7. Bhattacharyya, P.N., Jha, D.K., 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World Journal of Microbiology and Biotechnology 28(4): 1327–1350.
8. Bishop, M.L., Chang, A.C., Lee, R.W.K. 1994. Enzymatic mineralization of organic phosphorus in a volcanic soil in Chile. Soil Science 157(4): 238-243.

9. Cakmakci, R., Dönmez, M.F., Erdoğan, Ü., 2007. The effect of plant growth promoting rhizobacteria on barley seedling growth, nutrient uptake, some soil properties, and bacterial counts. Turkish Journal of Agriculture and Forestry 31(3): 189-199.
10. Calvo, P., Ormeño-Orrillo, E., Martínez-Romero, E., Zúñiga, D., 2010. Characterization of Bacillus isolates of potato rhizosphere from andean soils of Peru and their potential PGPR characteristics. Brazilian Journal of Microbiology 41(4): 899-906.
11. Caravaca, F., Figueroa, D., Roldán, A., Azcón-Aguilar, C., 2003. Alteration in rhizosphere soil properties of afforested Rhamnus lycioides seedlings in short-term response to mycorrhizal inoculation with Glomus intraradices and organic amendment. Environmental Management 31(3): 412-420.
12. 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. Applied Soil Ecology 34(1): 33-41.
13. Dinesh, R., Anandaraj, M., Kumar, A., Srinivasan, V., Bini, Y.K., Subila, K.P., Aravind, R., Hamza, S., 2013. Effects of plant growth-promoting rhizobacteria and NPK fertilizers on biochemical and microbial properties of soils under ginger (Zingiber officinale) cultivation. Agricultural Research 2(4): 346-353.
14. Egamberdieva, D., 2010. Growth response of wheat cultivars to bacterial inoculation in calcareous soil. Plant, Soil and Environment 56: 570-573.
15. Gianfreda, L., 2015. Enzymes of importance to rhizosphere processes. Journal of Soil Science and Plant Nutrition 15(2): 283-306.
16. Glick, B.R., Cheng, Z., Czarny, J., Duan, J., 2007. Promotion of plant growth by ACC deaminase-producing soil bacteria. European Journal of Plant Pathology 119(3): 329–339.
17. Goldstein, A. H. 1994. Involvement of the quinoprotein glucose dehydrogenises in the solubilization of exogenous phosphates by gram-negative bacteria. In: Phosphate in Microorganisms: Cellular and Molecular Biology, Torriani Gorini, A., Yagil, E., Silver, S. (Eds.). ASM Press, Washington DC, USA. pp. 197-203.
18. Gupta, N., Sabat, J., Parida, R., Kerkatta, D., 2007. Solubilization of tricalcium phosphate and rock phosphate by microbes isolated from chromite, iron and manganese mines. Acta Botanica Croatica 66(2): 197-204.
19. Hamadali, H., Hafidi, M., Virolle, M.J.., Ouhdouch, Y., 2008. Rock phosphate solubilizing actinomycetes: screening for plant growth promoting activities. World Journal of Microbiology and Biotechnology 24(11): 2565–2575.
20. Hamuda, H., Patkó, I., 2013. PGPR strains selection to improve plant productivity and soil quality. In: International Scientific-Practical Conference, Food, Technologies and Health 2013. 7-8 November 2013, Plovdiv, Bulgaria, Food Research and Development Institute, pp. 44-50.
21. Hinsinger, P., Bravin, M. N., Devau, N., Gerard, F., Le Cadre, E., & Jaillard, B. 2008. Soil-root microbe interactions in the rhizosphere: A key to understanding and predicting nutrient bioavailability to plants. Journal of Soil Science and Plant Nutrition 8:39-47.
22. Hussain, M.I., Asghar, H.N., Akhtar, M.J., Arshad, M., 2013. Impact of phosphate solubilizing bacteria on growth and yield of maize. Soil & Environment 32(1):71-78.
23. Karaca, A., Çetin, S.C., Turgay, O.C., Kızılkaya, R., 2011. Soil enzymes as indication of soil quality. In: Soil Enzymology, Soil Biology. Girish, S. Varma, A., (Eds.). Vol 22, Springer-Verlag Berlin Heidelberg. pp.119-148.
24. Khan, A.A., Jilani, G., Akhtar, M.S., Naqvi, S.M.S., Rasheed, M., 2009. Phosphorus solubilizing bacteria: occurrence, mechanisms and their role in crop production. Journal of Agricultural and Biological Sciences 1: 48-58.
25. Khan, M.S., Zaidi, A., Ahmad, E., 2014. Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Phosphate solubilizing microorganisms: Principles and application of microphos technology. Khan, M.S., Zaidi, A., Musarrat, J. (Eds.). Springer, Switzerland, pp. 31-62.
26. Kızılkaya, R., Aşkın, T., Bayraklı, B., Sağlam, M., 2004. Microbiological characteristics of soils contaminated with heavy metals. European Journal of Soil Biology 40(2): 95-102.
27. Kızılkaya, R., Bayraklı, B., 2005. Effects of N-enriched sewage sludge on soil enzyme activities. Applied Soil Ecology 30(3): 192-202.
28. Kohler, J., Caravaca, F., Carrasco, L., Roldán, A., 2007. Interactions between a plant growth-promoting rhizobacterium, an AM fungus and a phosphate-solubilising fungus in the rhizosphere of Lactuca sativa. Applied Soil Ecology 35(3): 480-487.
29. Kuan, K.B., Othman, R., Abdul Rahim, K., Shamsuddin, Z.H., 2016. Plant growth-promoting rhizobacteria inoculation to enhance vegetative growth, nitrogen fixation and nitrogen remobilisation of maize under greenhouse conditions. PLoS ONE 11(3): e0152478.
30. Lipping, Y., Jiatao, X., Daohong, J., Yanping, F., Guoqing, L., Fangcan, L., 2008. Antifungal substances produced by Penicillium oxalicum strain PY-1-potential antibiotics against plant pathogenic fungi. World Journal of Microbiology and Biotechnology 24(7): 909-915.
31. Majeed, A., Abbasi, M.K., Hameed, S., Imran, A., Rahim, N., 2015. Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Frontiers in Microbiology 6: 198.
32. Maliha, R., Khalil, S., Ayub, N., Alam, S., Latif, S., 2004. Organic acids production and phosphate solubilizaion by microorganisms (PSM) under in vitro conditions. Pakistan Journal of Biological Sciences 7(2): 187-196.
33. Mehrvarz, S., Chaichi, M.R., Alikhani, H.A., 2008. Effects of phosphate solubilizing microorganisms and phosphorus chemical fertilizer on yield and yield components of barely (Hordeum vulgare L.). American- Eurasian Journal of Agricultural Environmental Sciences 3(6): 822-828.
34. Mullen, M.D., 2005. Phosphorus in soils: Biological interactions. In: Encyclopedia of Soils in the Environment, Hillel, D., (Ed.). Elsevier, pp. 210–215.
35. Naseby, D.C., Lynch, J.M., 1997. Rhizosphere soil enzymes as indicators of perturbations caused by enzyme substrate addition and inoculation of a genetically modified strain of Pseudomonas fluorescens on wheat seed. Soil Biology and Biochemistry 29(9-10): 1353-1362.
36. Naseby, D.C., Moënne-Loccoz, Y., Powell, J., O‘Gara, F., Lynch, J.M., 1998. Soil enzyme activities in the rhizosphere of field-grown sugar beet inoculated with the biocontrol agent Pseudomonas fluorescens F113. Biology and Fertility of Soils 27(1): 39-43.
37. Ogut, M., Er, F., 2016.Mineral composition of field grown winter wheat inoculated with phosphorus solubilizing bacteria at different plant growth stages. Journal of Plant Nutrition 39(4): 479-490.
38. Ogut, M., Er, F., Kandemir, N., 2010. Phosphate solubilization potentials of soil Acinetobacter strains. Biology and Fertility of Soils 46(7): 707–715.
39. Roca, A., Pizarro-Tobías, P., Udaondo, Z., Fernández, M., Matilla, M.A., Molina-Henares, M.A., Molina, L., Segura, A., Duque, E., Ramos, J.L., 2013. Analysis of the plant growth-promoting properties encoded by the genome of the rhizobacterium Pseudomonas putida BIRD-1. Environmental Microbiology 15(3): 780–794.
40. Rowell, D.L., 1996. Soil Science: Methods and Applications. 3rd Edition Longman. London, UK.
41. Ryan, J., Estefan, G., Rashid, A., 2001. Soil and plant analysis laboratory manual. International Center for Agricultural Research in the Dry Areas (ICARDA). Syria.
42. Saharan, B.S., Nehra, V., 2011. Plant growth promoting rhizobacteria: a critical review. Life Sciences and Medicine Research Volume 2011: LSMR-21
43. Salantur, A., Ozturk, A., Akten, S., 2006. Growth and yield response of spring wheat (Triticum aestivum L.) to inoculation with rhizobacteria. Plant, Soil and Environment 52: 111-118.
44. Sarker, A., Talukder, N.M., Islam, Md.T., 2014. Phosphate solubilizing bacteria promote growth and enhance nutrient uptake by wheat. Plant Science Today 1(2): 86-93.
45. Sharma, S.B., Sayyed, R.Z., Trivedi, M.H., Gobi, T.A., 2013. Phosphate solubilising microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587.
46. Sharma, S.K., Johri, B.N., Ramesh, A., Joshi, O.P., Prasad, S.S., 2011. Selection of plant growth-promoting Pseudomonas spp. that enhanced productivity of soybean-wheat cropping system in central India. Journal of Microbiology and Biotechnology 21(11): 1127-1142.
47. Shenoy,V.V., Kalagudi, G.M., 2005. Enhancing plant phosphorus use efficiency for sustainable cropping. Biotechnology Advances 23(7-8): 501-513.
48. Singh, N., Kumar, S., Bajpai, V.K., Dubey, R.C., Maheshwari, D.K., Kang, S.C., 2010. Biological control of Macrophomina phaseolina by chemotactic fluorescent Pseudomonas aeruginosa PN1 and its plant growth promotory activity in chir-pine. Crop Protection 29(10): 1142–1147.
49. Son, T.T.N., Diep, C.N., Giang, T.T.M., 2006. Effect of bradyrhizobia and phosphate solubilizing bacteria application on soybean in rotational system in the Mekong delta. Omonrice 14: 48-57.
50. Song, O.R., Lee, S.J., Lee, Y.S., Lee, S.C., Kim, K.K., Choi, Y.L., 2008. Solubilization of insoluble inorganic phosphate by Burkholderia cepacia DA 23 isolated from cultivated soil. Brazil Journal of Microbiology 39(1): 151-156.
51. Souchie, E.L., Azcón, R., Barea, J.M., Saggin-Júnior, O.J., da Silva, E.M.R., 2007. Indolacetic acid production by P-solubilizing microorganisms and interaction with arbuscular mycorrhizal fungi. Acta Scientiarum Biological Sciences 29: 315-320.
52. Tank, N., Saraf, M., 2003. Phosphate solubilization, exopolysaccharide production and indole acetic acid secretion by rhizobacteria isolated from Trigonella graecum. Indian Journal of Microbiology 43(1): 37–40.
53. Taurian, T., Anzuay, M.S., Angelini, J.G., Tonelli, M.L., Ludueña, L., Pena, D., Ibáñez, F., Fabra, A., 2010. Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant and Soil 329(1): 421-431.
54. Toro, M., 2007. Phosphate solubilizing microorganisms in the rhizosphere of native plants from tropical savannas: An adaptive strategy to acid soils? In: Developments in Plant and Soil Sciences. Velaquez, C., Rodriguez-Barrueco, E., (Eds.). Springer, The Netherlands. pp. 249-252.
55. Trivedi, P., Sa, T. 2008. Pseudomonas corrugata (NRRL B-30409) mutants increased phosphate solubilization, organic acid production and plant growth at lower temperatures. Current Microbiology 56(2): 140–144.
56. Turan, M., Ekinci, M., Yildirim, E., Güneş, A., Karagöz, K., Kotan, R., Dursun, A. 2014. Plant growth-promoting rhizobacteria improved growth, nutrient, and hormone content of cabbage (Brassica oleracea) seedlings. Turkish Journal of Agriculture and Forestry 38: 327-333.
57. Ul Hassan, T., Bano, A., 2015. The stimulatory effects of L-tryptophan and plant growth promoting rhizobacteria (PGPR) on soil health and physiology of wheat. Journal of Soil Science and Plant Nutrition 15(1): 190-201.
58. Vassilev, N., Vasileva, M.A., Nikolaeva, L., 2006. Simultaneous P solubilizing and biocontrol activity of microorganisms: potentials and future trends. Applied Microbiology and Biotechnology 71(2): 137-144.
59. Vikram, A., Alagawadi, A.R., Hamzehzarghani, H., Krishnaraj, P.U., 2007. Factors related to the occurrence of phosphate solubilizing bacteria and their ısolation in vertisols. International Journal of Agricultural Research 2(7): 571-580.
60. Walker, J.D., Enache, M., Dearden, J.C.. 2003. Quantitative cationic activity relationships for predicting toxicity of metal ions from physicochemical properties and natural occurrence levels. QSAR & Combinatorial Science 26(4): 522–527.
61. Wang, X., Tang, C., Guppy, C.N., Sale, P.W.G., 2009. The role of hydraulic lift and subsoil P placement in P uptake of cotton (Gossypium hirsutum L.). Plant and Soil 325(1): 263–275.
62. Wani, P.A., Khan, M.S., Zaidi, A., 2007a. Co-inoculation of nitrogen fixing and phosphate solubilizing bacteria to promote growth, yield and nutrient uptake in chickpea. Acta Agronomica Hungarica 55(3): 315-323.
63. Wani, P.A., Khan, M.S., Zaidi, A. 2007b. Synergistic effects of the inoculation with nitrogen fixing and phosphate solubilizing rhizobacteria on the performance of field grown chickpea. Journal of Plant Nutrition and Soil Science 170(2): 283-287.
64. Wani, P.A., Khan, M.S., Zaidi, A., 2008. Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnology Letters 30(1): 159–163.
65. Xu, J.G., Johnson, R.L., 1995. Root growth, microbial activity and phosphatase activity in oil-contaminated, remediated and uncontaminated soils planted to barley and field pea. Plant and Soil 173(1): 3-10.
66. Yildirim, E., Turan, M., Donmez, M.F., 2008. Mitigation of salt stress in radish (Raphanus sativus L.) by plant growth promoting rhizobacteria. Roumanian Biotechnological Letters 13(5): 3933-3943.
67. Yildirim, E., Karlidag, H., Turan, M., Dursun, A., Goktepe, F., 2011a. Growth, nutrient uptake, and yield promotion of broccoli by plant growth promoting rhizobacteria with manure. HortScience 46(6): 932-936.
68. Yildirim, E., Turan, M., Ekinci, M., Dursun, A., Çakmakçı, R. 2011b. Plant growth promoting rhizobacteria ameliorate deleterious effect of salt stress on lettuce. Scientific Research and Essays 6(20): 4389-4396.
69. Zahid, M., Abbasi, M.K., Hameed, S., Rahim, M. 2015. Isolation and identification of indigenous plant growth promoting rhizobacteria from Himalayan region of Kashmir and their effect on improving growth and nutrient contents of maize (Zea mays L.). Frontiers in Microbiology 6: 207.