Advertisement

Applied Biological Chemistry

, Volume 60, Issue 3, pp 287–297 | Cite as

Biodegradation of endosulfan and pendimethalin by three strains of bacteria isolated from pesticides-polluted soils in the Sudan

  • Abd Elaziz Sulieman Ahmed Ishag
  • Azhari Omer Abdelbagi
  • Ahmed Mohammed Ali Hammad
  • Elsiddig Ahmed Elmustafa Elsheikh
  • Osama Elgilani Elsaid
  • Jang-Hyun Hur
Article

Abstract

Biodegradation of endosulfan (α and β) and pendimethalin by Bacillus safensis strain FO-36bT, Bacillus subtilis subsp. inaquosorum strain KCTC 13429T and Bacillus cereus strain ATCC14579T isolated from pesticides-polluted soil was studied in mineral salt medium. Endosulfan and pendimethalin were incubated with the three bacterial strains with samples drawn at various intervals for GC analysis. Representative samples were subject to GC–MS analysis. The loss in the initial concentrations, 0.663 mM (α endosulfan), 0.319 mM (β endosulfan) and 1.423 mM (pendimethalin), was monitored and used to compute the half-lives following biphasic model. Removal percentage of endosulfan and pendimethalin in the media inoculated with the bacterial strains ranged from 24 to 95% (α endosulfan), 21–91% (β endosulfan) and 51–97% (pendimethalin), respectively. Despite the significant decrease in starting material in B. safensis cultures, no metabolites were detected, whereas two major metabolites of endosulfan, 1,2,3,4,7,7-hexachloro-5,6-dihydroxybicyclo{2.2.1}-2-heptene and 1,2,3,4,7,7-hexachloro-formaldehyde-6-methylbicyclo{2.2.1}-2-heptene, were detected in the B. subtilis cultures, and one metabolite of pendimethalin metabolite; N-(1-ethylpropyl)-3-methyl-2, 6-diaminobenzine, was detected in the B. cereus culture. Generally, the result indicates the potential capability of these microorganisms in complete mineralization of endosulfan and pendimethalin. Based on half-lives, the efficiency of bacterial strains can be ordered as follows: B. subtilis > B. cereus > B. safensis for endosulfan and B. cereus > B. safensis > B. subtilis for pendimethalin.

Keywords

Biodegradation Endosulfan Isolation and identification Pesticide-contaminated soils Pendimethalin 

Notes

Acknowledgments

The authors would like to thank Mr. Adam Ali Mohamed and Mr. Salah of the National Chemical Laboratories, Federal Ministry of Health, Sudan, for their help with GC–MS analysis. The financial support made available by the Ministry of Higher Education and Scientific Research, Sudan, is highly acknowledged. The Korean Macrogen Company and Kangwon National University (KNU) were greatly acknowledged for their help with the identification of bacterial isolates by Molecular Biotechnology tools.

Supplementary material

13765_2017_281_MOESM1_ESM.docx (291 kb)
Supplementary material 1 (DOCX 291 kb)

References

  1. 1.
    Abdelbagi AO, Elmahi MA, Osman DG (2000) Chlorinated hydrocarbon insecticide residues in the Sudanese soils of limited or no pesticide use. Arab J Plant Protect 18:35–39Google Scholar
  2. 2.
    Abdelbagi AO, Elmahi MA, Osman DG (2003) Organochlorine insecticides residues in sudanese soils of intensive pesticide use and in surface soil of Qurashi pesticide store. UK J Agric Sci 11:59–68Google Scholar
  3. 3.
    Butrous (1999) Evaluation and assessment of obsolete and banned pesticides in five agricultural schemes. Report, 83–89, SudanGoogle Scholar
  4. 4.
    Abubaker OAW (2007) Level and movement of pesticide contaminants in the dangerous area of Port Sudan Harbour and their impact on human and aquatic life. Dissertation, University of KhartoumGoogle Scholar
  5. 5.
    Babiker M (1998) Levels and movement of some pesticides in Qurashi store area. Hessahisa province, central Sudan, Dissertation, University of KhartoumGoogle Scholar
  6. 6.
    Abdelbagi AO, Mohamed AA (2006) Pesticide residues in the Sudanese environment. In: Proceedings of a national workshop on measures for import, storage, handling and use of pesticides and fertilizers. Friendship Hall, Khartoum, Sudan. Organized by the Sudanese Standards and Metrology Organization, Khartoum. Sudan. Aug 2007. pp 66–118Google Scholar
  7. 7.
    Environmental Protection Agency (EPA) (1999) Persistent bioaccumulative toxic (PBT) chemicals. Final Rule, Fed. Regist 64, 58666 58753Google Scholar
  8. 8.
    Meister RT (1992) Farm chemicals handbook ‘92. Meister Publishing Company, WilloughbyGoogle Scholar
  9. 9.
    Environmental Protection Agency (1992) National study of chemical residues in fish: U.S. environmental protection agency, office of science and technology, EPA- 823-R-92-008b, v. 2, variously paged. Appendix 115Google Scholar
  10. 10.
    Ritter L, Solomon KR, Forget J, Stemeroff MO, Leary C (2007) Persistent organic pollutants: an assessment report on: DDT, aldrin, dieldrin, endrin, chlordane, heptachlor, hexachlorobenzene, mirex, toxaphene polychlorinated 13 biphenyls. Dioxins and furans, Prepared for The International Programme on Chemical Safety (IPCS)Google Scholar
  11. 11.
    Guerin TF (1999) The anaerobic degradation of endosulfan by indigenous microorganisms from low oxygen soils and sediments. Environ Pollut 106:13–21CrossRefGoogle Scholar
  12. 12.
    Shivaramaiah HM, Kennedy IR (2006) Biodegradation of Endosulfan by soil bacteria. J Enviorn Sci Health B 41:895–905CrossRefGoogle Scholar
  13. 13.
    Siddique T, Okeke BC, Arshad M, Frankenberger WT (2003) Enrichment and isolation of endosulfan-degrading microorganisms. JEQ 32:47–54Google Scholar
  14. 14.
    Shetty PK, Mitra J, Murthy NBK, Namitha KK, Sovitha KN, Raghu K (2000) Biodegradation of cyclodiene insecticide endosulfan by Mucor thermo---hyalospora MTCC 1384. Curr Sci 79:1381–1383Google Scholar
  15. 15.
    Elmahi MA (1996) Distribution of chlorinated hydrocarbon pesticides residues in Sudan soil. M.Sc. Dissertation, University of KhartoumGoogle Scholar
  16. 16.
    Ali TM (2005) Naturally occurring soil microorganism in qurashi pesticides store and the surrounding Gezira soil areas and their potential in degrading Endosulfan α, β and lindane. Dissertation, University of KhartoumGoogle Scholar
  17. 17.
    Elsaid OG, Abdelbagi AO, Elmustafa EA (2010) Microbial degradation of endosulfan in carbon free media and selective media. Res J Agric Biol Sci 6(3):257–562Google Scholar
  18. 18.
    Elsaid OG, Abdelbagi AO, Elsheikh EAE (2009) Effects of fertilizers (activators) in enhancing microbial degradation of endosulfan in soil. Res J Environ Toxicol 3(2):76–85CrossRefGoogle Scholar
  19. 19.
    Elsaid OG, Abdelbagi AO (2010) Comparative biodegradation of endosulfan by mutant and their native microorganisms. Res J Agric Biol Sci 6(6):953–961Google Scholar
  20. 20.
    Shaer IBS, Abdelbagi AO, Elmustafa EA, Ahmed SAI, Osama GE (2013) Biodegradation of pendimethalin by three strains of bacteria isolated from pesticides polluted soils. U K J Agric Sci 21(2):233–252Google Scholar
  21. 21.
    Ishag ASA, Abdelbagi AO, Hammad AMA, Elmustafa EA, Osama EE, Hur J-H, Laing MD (2016) Biodegradation of chlorpyrifos, malathion, and dimethoate by three strains of bacteria isolated from pesticide-polluted soils in Sudan. J Agric Food Chem 64:8491–8498CrossRefGoogle Scholar
  22. 22.
    Barrow GI, Feltham RKA (2003) Cowan, and steel’s manual for identification of medical bacteria, 3rd edn. Press Syndicate of the University of Cambridge, Cambridge, p 317Google Scholar
  23. 23.
    Thompson R, Marcelino A, Polz F (2002) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by ‘reconditioning PCR’. Nucleic Acids Res 30(9):2083–2088CrossRefGoogle Scholar
  24. 24.
    Tepper EZ, Shilnikova VK, pereverzeva GI (1994) A manual of Microbiology (In Russian), 4th Edition, kolas Publishers Moscow. 170 pGoogle Scholar
  25. 25.
    Gi-Seok K, Ho-Yong S, Kee-Sun S (2005) Biodegradation of the organochlorine insecticide, endosulfan, and the toxic metabolite, endosulfan sulfate, by Klebsiella oxytoca KE-8. Appl Microbiol Biotechnol 67:845–850CrossRefGoogle Scholar
  26. 26.
    Mathava K, Ligy P (2006) Endosulfan mineralization by bacterial isolates and possible degradation pathway identification. Bioremediat J 10(4):179–190CrossRefGoogle Scholar
  27. 27.
    Abdurruhman MA, Abdelbagi OA, Ahmed ASI (2015) Biodegradation of pendimethalin and atrazine by Pseudomonas pickettii isolated from pesticides polluted soil under laboratory conditions. J Biotechnol Sci Res 2(3):94–102Google Scholar
  28. 28.
    El Zorgani GA (1982) The status of DDT residues in Sudan. Progress report. Agricultural Research Corporation, Wad Medani, SudanGoogle Scholar
  29. 29.
    Kole RK, Saha J, Pal S, Chaudhuri S, Chowdhury A (1994) Bacterial degradation of the herbicide pendimethalin and activity evaluation of its metabolites. Bull Environ Contam Toxicol 52:779–786CrossRefGoogle Scholar
  30. 30.
    Thangadurai P, Suresh S (2014) Biodegradation of endosulfan by soil bacterial cultures. Int. Biodeterior. Biodegrad 94:38–49CrossRefGoogle Scholar
  31. 31.
    Byeoung-Soo P, Sung-Eun L (2004) Biotransformation of endosulfan by Anabaena sp. PCC 7120. Agric Chem Biotechnol 47(1):38–41Google Scholar
  32. 32.
    Singh SB, Kulshrestha G (1991) Microbial degradation of pendimethalin. J. Environ Sci Health B26:309–321CrossRefGoogle Scholar
  33. 33.
    Ulčnik A, Kralj CI, Pohleven F (2013) Degradation of lindane and endosulfan by fungi, fungal and bacterial laccases. World J Microbiol Biotechnol 29(12):2239–2247CrossRefGoogle Scholar
  34. 34.
    Megadi VB, Tallur PN, Hoskeri RS, Mulla SI, Ninnekar HZ (2010) Biodegradation of pendimethalin by Bacillus circulans. Indian J Biotechnol 9:173–177Google Scholar
  35. 35.
    Okerentugba PO, Ezeronye OU (2003) Petroleum degrading potentials of single and mixed microbial cultures isolated from rivers and refinery effluent in Nigeria. Afr J Biotechnol 2(9):288–292CrossRefGoogle Scholar
  36. 36.
    Elsaid OG, Abdelbagi AO, Elsheikh EAE (2011) Accelerating the rate of endosulfan degradation by bacteria and actinomycetes. Int J Appl Environ Sci 6(1):11–21Google Scholar
  37. 37.
    Singh PB, Sharma S, Saini HS, Chadha BS (2009) Biosurfactant production by Pseudomonas sp. and its role in aqueous phase partitioning and biodegradation of chlorpyrifos. Lett Appl Microbiol 49:378–383CrossRefGoogle Scholar
  38. 38.
    Khaled AO, Gamal HI, Ahamed IA, Abdul Rahman AA (2008) Biodegradation kinetics of dicofol by selected microorganisms. J Pest Biochem Physiol 91:180–185CrossRefGoogle Scholar
  39. 39.
    Rigas F, Papadopoulou K, Dritsa V (2007) Bioremediation of a soil contaminated by lindane utilizing the fungus Ganoderma austral via response surface methodology. J Hazard Mater 140(1–2):325–332CrossRefGoogle Scholar
  40. 40.
    Awasthi N, Manikam N, Kumar A (1997) Biodegradation of endosulfan by a bacterial co-culture. Bull Environ Contam Toxicol 59:928–934CrossRefGoogle Scholar
  41. 41.
    Jesitha K, Nimisha KM, Manjusha CM, Harikumar PS (2015) Biodegradation of endosulfan by Pseudomonas fluorescens. Environ Process 2(1):225–240CrossRefGoogle Scholar
  42. 42.
    Kullman SW, Matsumura F (1996) Metabolic pathway utilised by phanerochete chrysosporium for degradation of the cyclodiene pesticide endosulfan. Appl Environ Microbiol 62:593–600Google Scholar
  43. 43.
    Katayama A, Matsumura F (1993) Degradation of Organochlorine pesticides particularly endosulfan by Trichoderma harzianum. Environ Toxicol Chem 12:1059–1065CrossRefGoogle Scholar
  44. 44.
    Sutherland TD, Weir KM, Lacey MJ, Horne I, Russsel RJ, Oakeshott JG (2002) Enrichment of a microbial culture capable of degrading endosulphate, the toxic metabolite of endosulfan. J Appl Microbiol 92:541–548CrossRefGoogle Scholar
  45. 45.
    Miles JRW, May P (1979) Degradation of Endosulfan and it is Metabolites by Mixed Culture of Soil Microorganisms. Bull Environ Contam Toxicol 23:13–16CrossRefGoogle Scholar
  46. 46.
    Hai-yan N, Fei W, Na L, Li Y, Da Chen, Qin H, Jian H, Qing H (2016) The nitroreductase PNR is responsible for the initial step of pendimethalin degradation in Bacillus subtilis Y3. Appl Environ Microbiol. doi: 10.1128/AEM.01771-16 Google Scholar
  47. 47.
    Elsayed BB, El-Nady MF (2013) Bioremediation of pendimethalin-contaminated soil. Afr J Microbiol Res 7(21):2574–2588CrossRefGoogle Scholar

Copyright information

© The Korean Society for Applied Biological Chemistry 2017

Authors and Affiliations

  • Abd Elaziz Sulieman Ahmed Ishag
    • 1
  • Azhari Omer Abdelbagi
    • 1
  • Ahmed Mohammed Ali Hammad
    • 1
  • Elsiddig Ahmed Elmustafa Elsheikh
    • 2
  • Osama Elgilani Elsaid
    • 3
  • Jang-Hyun Hur
    • 4
  1. 1.Department of Crop Protection, Faculty of AgricultureUniversity of KhartoumShambatSudan
  2. 2.Department of Soil and Environment, Faculty of AgricultureUniversity of KhartoumShambatSudan
  3. 3.Faculty of Agricultural Technology and Fish SciencesAl Neelain UniversityKhartoumSudan
  4. 4.Department of Biological Environment, College of Agriculture and Life SciencesKangwon National UniversityChuncheonRepublic of Korea

Personalised recommendations