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Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by the epiphytic yeasts Rhodotorula glutinis and Rhodotorula rubra

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Abstract

The possible involvement of the epiphytic yeasts Rhodotorula glutinis and Rhodotorula rubra in the biodegradation of the insecticide chlorpyrifos and its metabolite 3,5,6-trichloro-2-pyridinol (TCP), in pure cultures and in plant surfaces (tomato fruits) was investigated. Higher biodegradation rates were observed as the concentration of chlorpyrifos and the inoculum of the microorganisms were increased, while the yeasts proved to be more active at 25 and 15 °C. The presence of glucose in the mineral nutrient medium, as an extra source of carbon, delayed the biodegradation by Rhodotorula glutinis, while Rhodotorula rubra proved to be more active. The detection and quantification of the parent compound and TCP was successfully achieved using a LC/MS/MS chromatographic system. The in vitro enzymatic assays applied suggested that esterases may be involved in the biodegradation of chlorpyrifos, a fact that was further enhanced after the addition of the synergists triphenyl phosphate, diethyl maleate and piperonyl butoxide in the biodegradation trials. The decrease of chlorpyrifos residues on tomato fruits confirmed the corresponding on pure cultures, resulting in the suggestion that the yeasts R. glutinis and R. rubra can possibly be used successfully for the removal or detoxification of chlorpyrifos residues on tomatoes.

Highlights

  • Biodegradation of chlorpyrifos by Rhodotorula glutinis and Rhodotorula rubra

  • Biodegradation of TCP by Rhodotorula glutinis and Rhodotorula rubra

  • Triphenyl phosphate inhibited the biodegradation of chlorpyrifos

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References

  • Abraham J, Silambarasan S (2013) Biodegradation of chlorpyrifos and its hydrolyzing metabolite 3,5,6-trichloro-2-pyridinol by Sphingobacterium sp. JAS3. Process Biochem 48(2013):1559–1564. https://doi.org/10.1016/j.procbio.2013.06.0341559–1564

    Article  CAS  Google Scholar 

  • Abraham J, Silambarasan S (2016) Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol using a novel bacterium Ochrobactrum sp. JAS2: A proposal of its metabolic pathway. Pestic Biochem Physiol 126(2016):13–21. https://doi.org/10.1016/j.pestbp.2015.07.001

    Article  CAS  Google Scholar 

  • Akbar S, Sultan S (2016) Soil bacteria showing a potential of chlorpyrifos degradation and plant growth enhancement. Braz J Microbiol 47:563–570. https://doi.org/10.1016/j.bjm.2016.04.009

    Article  CAS  Google Scholar 

  • Abu- Qare AW, Abou-Donia MB (2001) Determination of diazinon, chlorpyrifos and their metabolites in rat plasma and urine by high- performance liquid chromatography. J Chromatogr Sci 39(5):200–204

    Article  CAS  Google Scholar 

  • Anwar S, Liaquat F, Khan QM, Khalid ZM, Iqbal S (2009) Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol by Bacillus pumilus strain C2A1. J Hazard Mater 168(1):400–405. https://doi.org/10.1016/j.jhazmat.2009.02.059

    Article  CAS  Google Scholar 

  • Bempelou ED, Vontas JG, Liapis KS, Ziogas VN (2013) Biodegradation of diazinon by the epiphytic yeasts Rhodotorula glutinis and Rhodotorula rubra. Hellenic Plant Protection. Journal 6:69–82

    Google Scholar 

  • Bhagobaty RK, Joshi SR, Malik A (2007) Microbial degradation of organophosphorous pesticide: chlorpyrifos (mini-review) The Internet Journal of Microbiology 4(1):1–12

    Google Scholar 

  • Bauriedel WR (1986a). The Early Fate of 14 C-chlorpyrifos Applied to Leaf Surfaces of Corn, Soybean and Sugarbeat. DowElanco, Indianapolis, IN (unpublished report). In: Reviews of Environmental Contamination and Toxicology, Vol 131,Springer-Verla New York Inc. 1993. https://doi.org/10.1007/978-1-4612-4362-5

    Google Scholar 

  • Bilthoven (1996) Analytical Μethods for Pesticide Residues in Foodstuffs, Sixth edition. Ministry of Public Health, Welfare and Sport, The Netherlands, P. Van Zoonen (Ed), 4

    Google Scholar 

  • Bolognesi C, Moraso G (2000) Genotoxicity of pesticides: potential risk for consumers. Trends Food Sci Technol 11:182–187

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgramquantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–54

    Article  CAS  Google Scholar 

  • Chapman RA, Cole CM (1982) Observations on the ifluence of water and soil pH on the persistence of insecticides. J Environ Sci Health B 17:487–504

    Article  CAS  Google Scholar 

  • Chen S, Peng C, Hongmei L, Meiying H, Hu M, Zhong G (2012) Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol by a new fungal strain Cladosporium cladosporioides Hu-01. PLoS One 7(10):e47205. https://doi.org/10.1371/journal.pone.0047205.

    Article  CAS  Google Scholar 

  • Fang H, Xiang YQ, Hao YJ, Chu XQ, Pan XD, Yu JQ, Yu YL (2008) Fungal degradation of chlorpyrifos by verticillium sp. dsp in pure cultures and its use in bioremediation of contaminated soil and pachoi. Int Biodeterior Biodegrad 61:294–303

    Article  CAS  Google Scholar 

  • Fernadez MJ, Medrano L, Ruiz-Amil M, Losada M (1967) Regulation and function of pyruvate kinase and malate enzyme yeast. European J Biochem 3:11–18

    Article  Google Scholar 

  • Getzin LW (1981a) Degradation of chlorpyrifos in soil: influence of autoclaving, soil moisture and temperature. J Econ Entomol 74:158–162

    Article  CAS  Google Scholar 

  • Guha A, Kumari B, Bora TC, Roy MK (1997) Possible involvemrnt of plashmids in degradation of malathion and chlorpyrifos by micrococcus sp. Folia Microbiol 42(6):574–576

    Article  CAS  Google Scholar 

  • Havens PL, Rase HF (1991) Detoxification of Organophosphorus Pesticide Solutions. In: Tedder DW, Pohland FG (eds) Emerging technologies in Hazardous waste management II. ACS, Washington, DC, p 261–281

    Chapter  Google Scholar 

  • Horne I, Sutherland TD, Harcourt RL, Russel RJ, Oakeshott JG (2002) Identification of an opd (organophosphate degradation) Gene in Agrobacterium Isolate. Applied Environ Microbiol 68:3371–3376

    Article  CAS  Google Scholar 

  • Jones AS, Hastings FL (1981). Soil microbe srudies. In: Hastings F.L., Coster J.E. (eds). Field and laboratory evaluations of insecticides for southern pine beetle control. USDA. Southern Forest Experimental Station, Forest Service, SE, USA, 21, p 13–14, 35

  • Ivashina SA (1986) Interaction of Dursban with soil micro-organisms. Agrokhimia 8:75–76

    Google Scholar 

  • Koch HM, Angerer J (2001) Analysis of 3,5,6-trichloro-2-pyridinol in Urine Samples from the General Population Using Gas Chromatography- Mass Spectrometry after Steam Distillation and Solid Phase Extraction. J Chromatogr B 759:43–49

    Article  CAS  Google Scholar 

  • Lakshmi CV, Kumar M, Khanna S (2008) Biotransformation of chlorpyrifos and bioremediation of contaminate soil. Int Biodeterior Biodegrad 62:204–209

    Article  CAS  Google Scholar 

  • Lal S, Lal R (1987) Bioaccumulation, metabolism and effects of DDT, fenitrothion and chlorpyrifos on Saccharomyces cerevisae. Arch Environm Contam Toxicol 16:753–757

    Article  CAS  Google Scholar 

  • Li X, He J, Li S (2007) Isolation of a chlorpyrifos-degrading bacterium, Sphingomonas sp. strain Dsp-2 and cloning of the mpd Gene. Res Microbiol 158:143–149

    Article  CAS  Google Scholar 

  • Lu P, Li Q, Liu H, Feng Z, Yan X, Hong Q, Li S (2013) Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by Cupriavidus sp. DT-1 Bioresour Technol. 127:337–42

    Article  CAS  Google Scholar 

  • Mallick K, Bharati K, Banerji A, Shakil NA, Sethunathan N (1999) Bacterial degradation of chlorpyrifos in pure cultures and in soil. Bull Environ Contam Toxicol 62:48–54

    Article  CAS  Google Scholar 

  • Meikle RW, Youngson CR (1978) The hydrolysis rate of chlorpyrifos [O,O-diethyl O-(3,5,6-trichloro-2-pyridyl)-phosphorothiorate] and its dimethyl analog, chlorpyrifos methyl, in dilute aqueous solution. Arch Environ Contam Toxicol 7:13–22

    Article  CAS  Google Scholar 

  • McCall PJ (1986a) Hydrolysis of Chlorpyrifos in Dilute Aqueous Solution. DowElanco, Indianapolis, IN

    Google Scholar 

  • Medrano L, Ruiz-Amil M, Losada M (1969) Effect of glucose on pyruvate utilization by Rhodotorula glutinis. Arch Microbiol 66:239–249

    CAS  Google Scholar 

  • Muncnerova D, Augustin J (1995) Assimilation of benzoate by rhodotorula rubra, rhodotorula glutinis and rhodosporidium toluroides, as affected by glucose or xylose. World J Microbiol Biotechnol 11:240–241

    Article  CAS  Google Scholar 

  • Mulbry WW, Karns JS, Kearney PC, Nelson JO, McDaniel CS, Wild JR (1986) Identification of a plasmid-borne parathion hydrolase gene from flavobacterium sp. by southern hybridization with opd from pseudomonas diminuta. Applied Environ Microbiol 51:926–930

  • Racke KD (1993) Environmental fate of Chlorpyrifos. Rev Environ Contam Toxicilogy 131:1–151

    CAS  Google Scholar 

  • Racke KD, Coats JR, Titus KR (1988) Degradation of chlorpyrifos and its hydrolysis products 3,5,6-trichloro-2-pyridinol, in Soil. J Environ Sci Health B 23:527–539

    Article  Google Scholar 

  • Roditakis E, Grispou M, Morou E, Kristoffersen JB, Roditakis N, Nauen R, Vontas J, Tsagkarakou A (2009) Current status of insecticide resistance in Q biotype Bemisia tabaci populations from Crete. Pest Manag Sci 65(3):313–22

    Article  CAS  Google Scholar 

  • Ruiz-Amil M, Torrontegui G, Palacian E, Catalina L, Losada M (1965) Properties and functions of yeast puryvate carboxylase. J Biol Chem 240:3485–3492

    CAS  Google Scholar 

  • Sancho JV, Pozo OJ, Hernandez F (2000) Direct determination of chlorpyrifos and its main metabolite 3,5,6-trichloro-2-pyridinol in human serum and urine by coupled-column liquid chromatography/electrospray-tandem mass spectrometry. Rapid Commun Mass Spectrom 14:1485–1490

    Article  CAS  Google Scholar 

  • SANTE/11945/2015. Commission of the European Union, Doc No SANTE/11945/2015. Guidance document on analytical quality control and method validation procedures for pesticides residues analysis in food and feed

  • SAS Institute (2008) SAS/STAT guide for personal computers, version 8 Ed SAS Institute, Cary, p 333

  • Serdar CM, Gibson DT, Munnecke DM, Lancaster JH (1982) Plasmid involment in parathion hydrolysis by pseudomonas diminuta. Applied Environ Microbiol 44:246–249

    CAS  Google Scholar 

  • Shaker N, Abo-Donia S, El-Shaheed YA, και Ismail (1988) Effect of lactic acid bacteria and heat treatments on pesticides contaminated milk Egypt J Diary Sci 16:309–317

  • Silambarasan, S. and Abraham, J. (2013). Ecofriendly method for bioremediation of chlorpyrifos from agricultural soil by novel fungus Aspergillus terreus JAS1. Water Air and Soil Pollution, 224(1). https://doi.org/10.1007/s11270-012-1369-0

  • Silambarasan, S. and Abraham, J. (2014). Efficacy of Ganoderma sp. JAS4 in bioremediation of chlorpyrifos and its hydrolyzing metabolite TCP from agricultural soil. Journal of Basic Microbiology 54(1). https://doi.org/10.1002/jobm201200437

  • Singh BK, Walker A, Morgan JAW, Wright DJ (2004) Biodegradation of chlorpyrifos by enterobacter strain-B14 and Its use in bioremediation of contaminated soils. Applied Environ Microbiol 70(8):4855–4863

    Article  CAS  Google Scholar 

  • Singh BK, Walker A, Wright DJ (2006) Bioremedial potential of fenamiphos, chlorpyrifos, degrading isolates: influence of different environmental conditions. Soil Biol Biochem 38:2682–2693

    Article  CAS  Google Scholar 

  • Tomlin C, (2003) The Pesticide Manual, 13th edition, British Crop Protection Council. UK (Omega Park, Alton, Hampshire GU34 2QD)

  • Torrontegui G, Palacian E, Losada M (1966) Phosphoenolpyruvate carboxykinase in gluconeogenesis and itsrepression by hexoses in yeasts. Biochem Biophys Res Commun 22:227–231

    Article  Google Scholar 

  • Vontas JG, Small GJ, Hemingway J (2001) Glutathione S-transferases as antioxidant defense agents confer pyrethroid resistance in N. lugens. Biochem J 357:65–72

    Article  CAS  Google Scholar 

  • Xu G, Zheng W, Li Y, Wang S, Zhang J, Yan Y (2008) Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by newly isolated paracoccus sp. Straun TRP. Int Biodeterior Biodegrad 62:51–56

    Article  CAS  Google Scholar 

  • Yang L, Zhao YH, Zhang BX, Yang CH, Zhang X (2005) Isolation and characterization of A chlorpyrifos and 3,5,6-trichloro-2-pyridinol degrading Bacterium. FEMS Microbiol Lett 251:67–73

    Article  CAS  Google Scholar 

  • Yang C, Liu N, Guo X, Qiao C (2006) Cloning of Mpd gene from a chlorpyrifos-degrading bacterium and use of this strain in bioremediation of contaminated soil. FEMS Microbiol Lett 265:118–125

    Article  CAS  Google Scholar 

  • Yu YL, Fanf H, Wang X, Wu XM, Shan M, Yu JQ (2006) Characterization of a fungal strain capable of degrading chlorpyrifos and its use in detoxification of the insecticide on vegetables Biodegradation 17:487–494

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Our study entitled “Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by the epiphytic yeasts Rhodotorula glutinis and Rhodotorula rubra”, was not funded.

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Correspondence to E. D. Bempelou.

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Bempelou, E.D., Vontas, J.G., Liapis, K.S. et al. Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by the epiphytic yeasts Rhodotorula glutinis and Rhodotorula rubra. Ecotoxicology 27, 1368–1378 (2018). https://doi.org/10.1007/s10646-018-1992-7

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