Bioremediation of Certain Organophosphorus Pesticides by Two Biofertilizers, Paenibacillus( Bacillus) polymyxa (Prazmowski ) and Azospirillum lipoferum (Beijerinck)

Authors
1 Department of Plant Production, Faculty of Technology and Development, Zagazig University, Zagazig, Egypt.
2 Department of Plant Protection, Faculty of Agriculture, Zagazig University, Zagazig, Egypt.
Abstract
Continuous and excessive use of organophosphorus compounds has led to the contamination of water and soil ecosystems. The degradation of organophosphorus insecticides, chlorpyrifos, chlorpyrifos- methyl, cyanophos and malathion in mineral salts media were studied. The effect of additional biofertilizers, singly or combined with organic amendments, on chlorpyrifos and cyanophos degrading activity in soil were investigated. Paenibacillus ( Bacillus) polymyxa (Prazmowski ) and Azospirillum lipoferum (Beijerinck) were found to degrade the organophosphorus insecticides, chlorpyrifos, chlorpyrifos- methyl, cyanophos and malathion in mineral salts media as a carbon and phosphorus source. Paenibacillus ( Bacillus) polymyxa (Prazmowski ) appeared to be more effective than Azospirillum lipoferum in degrading all the tested organophosphate pesticides in mineral salts media. The half-life values (t1/2) of chlorpyrifos, chlorpyrifos – methyl , cyanophos and malathion were found to be undetectable , undetectable , 2.4, and undetectable days in mineral salts media inoculated by Paenibacillus ( Bacillus) polymyxa (Prazmowski ),while they reached 1.6, 0.1, 5.2, and 0.8 days by Azospirillum lipoferum (Beijerinck) compared to 4.4, 1.8, 8.8, and 1.4 days in non-inoculated mineral salts media. Chlorpyrifos and cyanophos degraded in soil samples inoculated by Azospirillum lipoferum (Beijerinck) plus peat- moss more rapidly than in the other treatments. Dual inoculation of Azospirillum lipoferum (Beijerinck) and Paenibacillus ( Bacillus) polymyxa (Prazmowski ) improved the rate of degradation of chlorpyrifos and cyanophos in soil. Azospirillum lipoferum (Beijerinck) appeared to be more effective than Paenibacillus ( Bacillus) polymyxa (Prazmowski ) in degrading soil-applied chlorpyrifos and cyanophos. These results highlight the potential of these bacteria to be used in the clean- up of contaminated pesticides – waste in the environment.

Keywords


1. Alexander, M. 2000. Aging Bioavailability and Overestimation of Risk from Environmental Pollutants. Environ. Sci. Technol., 34: 4259-4265.
2. Aronstein, B. N., Calvillo, Y. M. and Alexander, M. 1991. Effect of Surfactants at Low Concentration on the Desorption and Biodegradation of Sorbed Aromatic Compounds. Environ. Sci. Technol., 25: 1722-1731.
3. Awad, N. S., Sabit, H. H., Abo-Aba, S. E. M. and Bayoumi, R. A. 2011. Isolation, Characterization and Fingerprinting of Some Chlorpyrifos-Degrading Bacterial Strains Isolated from Egyptian Pesticides-polluted Soils. Afr. J. Microbiol. Res., 5: 2855-2862.
4. Barcelo, D. 1991. Occurance, Handling and Chromatographic Determination of Residues in the Aquatic Environment. Analyst, 116: 681-689.
5. Bending, G. D., Rodriguez-Cruz, M. S. and Lincoln, S. D. 2007. Fungicide Impacts on Microbial Communities in Soils with Contrasting Management histories. Chemosphere, 69: 82–88.
6. Bo, L., Ying-hua, Z. and Xin-huai, Z. 2011. Degradation Kinetics of Seven Organophosphorus Pesticides in Milk during Yoghurt Processing. J. Serb. Chem. Soc., 76: 1–10.
7. Chiba, M., Shlgeru, K. and Izuru, Y. 1976. Metabolism of Cyanox and Surecide in Bean Plants and Degradation in Soil. J. Pesticide. Sci, 1: 179-191
8. Cisar, J. L. and Snyder, G. H. 2000. Fate and Management of Turf Grass Chemicals. ACS Symp Series, 743: 106–126.
9. Datta, M., Banik, S. and Lasker, S. 1992. Effect of Inoculation of Phosphate Dissolving Bacteria on Rice (Oryza sativa) in Acid Soil. Indian J. Agric. Sci., 62(7): 482-485.
10. EL-Kabbany, S. 2002. Evaluation of Our Biofertilizer, for Bioremediation of Pesticide Contaminated Soil. The First Conf. of the Central Agric. Pesticide Lab., Sept. 3-5, Ministry of Agriculture and Land Reclamation, Agriculture Research Centre, Giza, Egypt.
11. El-Mancy, M. and Kotb, M. 2006. Biological and chemical phosphatic fertilization effects on wheat crop. J. product. Dev., 11(1): 103-121.
12. Fang, H., Xiang, Y. Q. and Hao, Y. J. 2008. Fungal Degradation of Chlorpyrifos by Verticillium sp. DSP in Pure Cultures and Its Use in Bioremediation of Contaminated Soil and Pakchoi. Int. Biodeteri. Biodegr., 61: 294–303.
13. Floesser-Mueller, H. and Swack, W. 2001. Photochemistry of Organophosphorus Insecticides. Rev. Environ. Contam. Toxicol., 172: 129–228.
14. Frenich, A., Rodriguez, J., Vidal, J., Arrebola, F. and Torres, M. 2005. A Study of the Disappearance of Pesticides during Composting Using a Gas Chromatography-tandem Mass Spectrometry Technique. Pest. Manage. Sci., 61: 458-466.
15. Ghanem, I., Orfi, M. and Shamma, M. 2007. Biodegradation of Chlorpyrifos by Klebsiella sp. Isolated from an Activated Sludge Sample of Waste Water Treatment Plant in Damascus. Folia. Microbiol., 52: 423–427.
16. Gu, J. G., Qlaa, C. L. and Gu, J. D. 2003. Biodegradation of the Herbicides Atrazine, Cyanazine, and Dicamba by Methanogenic Enrichment Cultures from Selective Soils of China. Bull. Environ. Contam. Toxicol., 71: 924-93.
17. Gunalan, P. H. and Fournier, C. 1993. Effect of Microbial Competition on the Survival and Activity of 2,4-D-degrading Alcaligenes xylosoxidans sub sp. denitrificons Added to Soil. Letters Appl. Microbiol.,16: 178-181.
18. Howard, P. H. 1991. Handbook of Environmental Fate and Exposure Data for Organic Chemicals: Pesticides. Lewis Publishers, Chelsea, MI, 3: 5-13.
19. Hong, S. H., Ryu, H., Kim, J. and Cho, K. S. 2011. Rhizoremediation of Diesel-contaminated Soil Using the Plant Growth-promoting Rhizobacterium Gordonia sp. S2RP-17. Biodegradation, 22: 593–601.
20. Huang, X. D., El-Alawi, Y., Penrose, D. M., Glick, B. R. and Greenberg, B. M. 2004. A Multi-process Phytoremediation System for Removal of Polycyclic Aromatic Hydrocarbons from Contaminated Soils. Environ. Pollut., 130: 465–476.
21. Illmer, P. and Schinner, F. 1995. Solubilization of Inorganic Calcium Phosphates-solubilization Mechanisms. Soil. Biol. Biochem., 27: 257-263.
22. Jiang, C. Y., Sheng, X. F., Qian, M. and Wang, Q. Y. 2008. Isolation and Characterization of a Heavy Metal-resistant Burkholderia sp. from Heavy Metal-contaminated Paddy Field Soil and Its Potential in Promoting Plant Growth and Heavy Metal Accumulation in Metal-polluted Soil. Chemosphere, 72: 157–164.
23. Joseph, D. E. and Dube, J. N. 1988. Growth Pattern of Azospirillum brasilense in Coal- and Soil-based Carriers. Geobios, 15: 191-192.
24. Kanade, S. N., Ade, A. B. and Khilare, V. C. 2012. Malathion Degradation by Azospirillum lipoferum Beijerinck. Sci. Res. Reporter, 2(1): 94-103.
25. Karpouzas, D. G. and Walker, A. 2000 Factors Influencing the Ability of Pseudomonas putida epI to Degrade Ethoprophos in Soil. Soil Biol. Biochem., 32: 1753-1762.
26. Kazemi, M., Tahmasbi, A. M., Valizadeh, R., Naserian, A. A. and Soni, A. 2012. Organophosphate Oesticides: A General Review. Agric. Sci. Res. J., 2: 512- 522.
27. Khaled, A. O., Gamal, A. H., Ahmad, I. A. and Abdul Rahman, A. A. 2008. Biodegradation Kinetics of Dicofol by Selecting Microorganisms. Pestic. Biochem. Physiol., 91: 180–185.
28. Kloepper, J. W., Ryu, C. M. and Zhang, S. 2004. Induced Systemic Resistance and Promotion of Plant Growth by Bacillus spp. Phytopathol., 94: 1259–1266.
29. Krause, M., Loubser, J. T. and De-Beer, P. R. 1986. Residues of Aldicarb and Fenamiphos in Soil. J. Agric. Food. Chem., 34: 717-720.
30. Krishna, K. 2002. Soil Fertility and Crop Production. Science Publishers, Inc. Enfield, NH, USA, 289 PP.
31. Kulshrestha, G. and Kumari, A. 2011. Fungal Degradation of Chlorpyrifos by Acremonium sp. Strain (GFRC-1) Isolated from a Laboratory-enriched Red Agricultural Soil. Biol. Fert. Soils, 47: 219-225.
32. Lai, K., Stolowich, N. J. and Wild, J. R. 1995. Characterization of P–S Bond Hydrolysis in Organophosphorothioate Pesticides by Organophosphorus Hydrolase. Arch. Biochem. Biophys., 318: 59–64.
33. Liu, Z., Chen, X., Shi, Y. and Su, Z. 2012. Bacterial Degradation of Chlorpyrifos by Bacillus cereus. Adv. Mater. Res., 356: 676-680.
34. Mallick, K., Bharati, K., Banerji, A. and Sethunathan, N, 1999. Bacterial Degradation of Chlorpyrifos in Pure Culture and in Soil. Bull. Environ. Contam. Tocxicol., 62: 48-54.
35. Massiha, A., Majid, M. R., Pahlaviani1, K. and Issazadeh, K. 2011. Microbial Degradation of Pesticides in Surface Soil Using Native Strain in Iran. In: "Int. Conf. Biotechnol. Environ. Manag.". IPCBEE, IACSIT Press, Singapore, 18: 76-81.
36. Mulbry, W. W., Ahrens, E. and Karns, J.S.1998. Use of a Field Scale Biofilter for the Degradation of the Organophosphate Insecticide Coumaphos in Cattle Dip Wastes. Pestic. Sci., 52: 268-274.
37. Mulchaldani A., Kaneva, I. and Chen, W. 1999. Detoxifi‌cation of Organophosphate Pesticides by Immobilized Escherichia coli Expressing Organophosphorus Hydro‌lase on Cell Surface. Biotechnol. Bioeng., 63: 216-223.
38. Myresiotis, C. K. and Vryzas, Z. 2012. Biodegradation of Soil-applied Pesticides by Selected Strains of Plant Growth-promoting Rhizobacteria (PGPR) and Their Effects on Bacterial Growth. Biodegradation, 23: 297–310.
39. Ortiz-hernández, M. L and Enrique, S. 2010. Biodegradation of the Organophosphate Pesticide Tetrachlorvinphos by Bacteria Isolated from Agricultural Soils in México. Rev. Int. Contam. Ambient, 26 :27-38.
40. Osman, K. A., Ibrahim, G. H., Askar, A. I. and Aba Alkhail, A. R. 2008. Biodegradation Kinetics of Dicofol by Selected Microorganisms. Pestic. Biochem. Physiol., 91: 180–185.
41. Qiao, C. L., Huang, J. Li, X., Shen, B. and Zhang, J. L. 2003. Bioremediation of Organophosphate Polluants by a Genetically Engineered Enzyme. Bull. Environ. Contam. Tocxicol., 70: 455-461.
42. Racke, K. D., Laskowski, D. A. and Schultz, M. R. 1990. Resistance of Chlorpyrifos to Enhanced Biodegradation in Soil. J. Agric. Food. Chem., 38: 1430-1436.
43. Racke K. D., Coats J. R., Titus K. R. 1988. Degradation of Chlorpyrifos and Its Hydrolysis Products, 3, 5, 6-trichloro-2- pyridinol, in Soil. J. Environ. Sci. Health B. 23: 527-539
44. Racke, K. D., Steele, K. P., Yoder, R. N., Dick, W. A. and Avidov, E. 1996. Factors Effecting the Hydrolytic Degradation of Chlorpyrifos in Soil. J. Agric. Food Chem., 44: 1582–1592.
45. Raveh, L., Segall, Y., Leader, H., Rothschild, N., Levanon, D., Henis, Y. and Ashani, Y. 1992. Protection against Tabun Toxicity in Mice by Prophylaxis with an Enzyme Hydrolyzing Organophosphate Esters. Biochem. Pharmacol., 44: 397–400.
46. Requena, N., Baca, T. M. and Azcon, R. 1997. Evaluation of Humic Substances from Unripe Compost during Incubation with Lignolytic or Cellulytic Microorganisms and Effects on the Lettuce Growth Promotion Mediated by Azotobacter chroococcum. Biol. Fertil. Soils, 24: 95-65.
47. Roodveldt, C. and Tawfik, D. S. 2005. Directed Evolution of Phosphotriesterase from Pseudomonas diminuta for Heterologous Expression in Escherichia coli Results in Stabilization of the Metal-free State. Protein Eng. Des. Sel., 18: 51–58.
48. Scott, C., Pandey, G., Hartley, C. J., Jackson, C. J., Cheesman, M. J., Taylor, M. C., Pandey, R., Khurana, J. L., Teese, M., Coppin, C. W., Weir, K. M., Jain, R. K., Lal, R., Russell, R. J. and Oakeshott, J. G. 2008. The Enzymatic Basis for Bioremediation. Indian J. Microbiol., 48: 65-79.
49. Singh, B. K. and Walker, A. 2006. Microbial Degradation of Organophosphorus Compounds. FEMS Microbiol. Rev., 30: 428-471.
50. Singh, B. K., Walker, A., Morgan, J. A. W., and Wright, D. J. 2003. Effects of Soil pH on the Biodegradation of Chlorpyrifos and Isolation of a Chlorpyrifos-Degrading Bacterium. Appl. Environ. Microbiol., 69: 5198-5206.
51. Singh, B. K., Walker, A., Alun, J., Morgan, W. and Wright, D. J.2004. Biodegradation of Chlorpyrifos by Enterobacter Strain B-14 and Its Use in Bioremediation of Contaminated Soils. Appl. Environ. Microbial., 70(8): 4855-4863.
52. Singh, B., Walker, A. and Wright, D. J. 2005. Cross-enhancement of Accelerated Biodegradation of Organophosphorus Compounds in Soils: Dependence on Structural Similarity of Compounds. Soil. Biol. Biochem., 37: 1675-1682.
53. Singh, B. K., Walker, A. and Wright, D. J. 2006. Bioremedial Potential of Fenamiphos and Chlorpyrifos Degrading Isolates: Influence of Different Environmental Conditions. Soil Biol. Biochem., 38: 2682-2693.
54. Singh, D. P., Khattar, J. I., Nadda, J. and Singh, Y. 2011. Chlorpyrifos Degradation by the Cyanobacterium synechocystis sp. Strain PUPCCC 64. Environ. Sci. Pollut. Res., 18: 1351–1359.
55. Srinivasulu, M., Jaffer, G., Madakka, M. and Rangaswamy, V. 2012. Effect of Pesticides on the Population of Azospirillum sp. and on Ammonification Rate in Two Soils Planted to Groundnut (Arachis hypogaea L.). Tropical. Ecology, 53: 93-104.
56. Tse, H., Comba, M. and Alaee, M. 2004. Methods for the Determination of Organophosphate Insecticides in Water, Sediments and Biota. Chemosphere, 54: 41–47.
57. Van Loon, L. C. 2007. Plant Responses to Plant Growth-promoting Rhizobacteria. Eur. J. Plant Pathol., 119: 243–254.
58. Van Veen, J. A., Van- Ovdrbeek, L.S. and Van Elsas, J. D. 1997. Fate and Activity of Microorganisms Introduced into Soil. Microbiol. Mol. Biol. Rev., 61:121-135.
59. Vidya, L. C., Kumar, M. and Khanna, S.2009. Biodegradation of Chlorpyrifos in Soil by Enriched Cultures. Current. Microbiol., 58(1): 35–38.
60. Vryzas, Z., Emmanuil N. P., Katerina, O., Theodoros, P. M. and Euphemia, P. 2012. Biotransformation of Atrazine and Metolachlor within Soil Profile and Changes in Microbial Communities. Chemosphere, 89: 1330–1338.
61. Wang, M. C., Liu, Y. H., Wang, Q., Gong, M., Hua, X. M., Pang, Y. J., Hu, S. and Yang, Y. H. 2008. Impacts of Methamidophos on the Biochemical, Catabolic, and Genetic Characteristics of Soil Microbial Communities. Soil Biol. Biochem., 40: 778–788.
62. Watkins, L. M., Mahoney, H. J., McCulloch, J. K. and Raushel, F. M. 1997. Augmented Hydrolysis of Diisopropyl Fluorophosphate in Engineered Mutants of Phosphotriesterase. J. Biol. Chem., 272: 25596–25601.
63. Wauchope, R. D., Buttler, T. M., Hornsby, A. G., Augustijn-Beckers, P. W. M. and Burt, J. P. 1992. SCS/ARS/CES Pesticide Properties Database for Environmental Decisionmaking. Rev. Environ. Contam. Toxicol., 123: 5-20.
64. Weber, J. R. and Huang, W. 1996. A Distributed Reactivity Model for Sorption by Soil and Sediments. 4. Intraparticle Heterogeneity and Phase-distribution Relationships under Non Aquilibrium Conditions. Environ. Sci. Technol., 30: 881-888.
65. Worthing, C. R. and Hance, R. J. 1991. The Pesticide Manual. British Crop Protection Council, Farnham.
66. Yang, L., Zhao, Y. H. and Zhang, B. X. 2005. Isolation and Characterization of a Chlorpyrifos and 3,5,6-trichloro-2-pyridinol Degrading Bacterium. FEMS Microbiol. Letters, 251: 67– 73.
67. Zhuang, X., Chen, J., Shim, H. and Bai, Z. 2007. New Advances in Plant Growth-promoting Rhizobacteria for Bioremediation. Environ. Int., 33: 406–413.
68. Zhu, J., Zhao, Y. and Qiu, J. 2010. Isolation and Application of a Chlorpyrifos-degrading Bacillus licheniformis ZHU-1. Afr. J. Microbiol. Res., 4: 2410-2413.