Abstract
The ability of pure manganese peroxidase (MnP), laccase, lignin peroxidase (LiP) and horseradish peroxidase (HRP) to degrade the widely used herbicide glyphosate and other pesticides was studied in separate in vitro assays with addition of different mediators. Complete degradation of glyphosate was obtained with MnP, MnSO4 and Tween 80, with or without H2O2. In the presence of MnSO4, with or without H2O2, MnP also transformed the herbicide, but to a lower rate. Laccase degraded glyphosate in the presence of (a) 2,2′-azino-bis(3-ethylbenzthiazoline-6-sulphonic acid) (ABTS), (b) MnSO4 and Tween 80 and (c) ABTS, MnSO4 and Tween 80. The metabolite AMPA was detected in all cases where degradation of glyphosate occurred and was not degraded. The LiP was tested alone or with MnSO4, Tween 80, veratryl alcohol or H2O2 and in the HRP assay the enzyme was added alone or with H2O2 in the reaction mixture. However, these enzymes did not degrade glyphosate. Further experiments using MnP together with MnSO4 and Tween 80 showed that the enzyme was also able to degrade glyphosate in its commercial formulation Roundup® Bio. The same enzyme mixture was tested for degradation of 22 other pesticides and degradation products present in a mixture and all the compounds were transformed, with degradation percentages ranging between 20 and 100%. Our results highlight the potential of ligninolytic enzymes to degrade pesticides. Moreover, they suggest that the formation of AMPA, the main metabolite of glyphosate degradation found in soils, can be a result of the activity of lignin-degrading enzymes.
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Arias ME, Arenas M, Rodriguez J, Soliveri J, Ball AS, Hernandez M (2003) Kraft pulp biobleaching and mediated oxidation of a nonphenolic substrate by laccase from Streptomyces cyaneus CECT 3335. Appl Environ Microbiol 69(4):1953–1958. doi:10.1128/AEM.69.4.1953-1958.2003
Barr D, Aust S (1994) Pollutant degradation by white rot fungi. Rev Environ Contam Toxicol 138:49–72
Barry G, Kishore G, Padgette S, Taylor M, Kolacz K, Weldon M, Re D, Eichholtz D, Fincher K, Hallas L (1992) Inhibitors of amino acid biosynthesis: strategies for imparting glyphosate tolerance to crop plants. In: Singh B, Flores H, Shannon J (eds) Biosynthesis and molecular regulation of amino acids in plants. American Society of Plant Physiologists, Rockville, pp 139–145
Bhunia A, Durani S, Wangikar PP (2001) Horseradish peroxidase catalyzed degradation of industrially important dyes. Biotechnol Bioeng 72(5):562–567. doi:10.1002/1097-0290(20010305)72:5<562::AID-BIT1020>3.0.CO;2-S
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54(1):519–546. doi:10.1146/annurev.arplant.54.031902.134938
Böhmer S, Messner K, Srebotnik E (1998) Oxidation of phenanthrene by a fungal laccase in the presence of 1-hydroxybenzotriazole and unsaturated lipids. Biochem Biophys Res Commun 244(1):233. doi:10.1006/bbrc.1998.8228
Borggaard OK, Gimsing AL (2008) Fate of glyphosate in soil and the possibility of leaching to ground and surface waters: a review. Pest Manag Sci 64(4):441–456. doi:10.1002/ps.1512
Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 267(1):99–102. doi:10.1016/0014-5793(90)80298-W
Bujacz B, Wieczorek P, Krzysko-Lupicka T, Golab Z, Lejczak B, Kavfarski P (1995) Organophosphonate utilization by the wild-type strain of Penicillium notatum. Appl Environ Microbiol 61(8):2905–2910
Castillo MdP, Torstensson L (2007) Effect of biobed composition, moisture, and temperature on the degradation of pesticides. J Agric Food Chem 55(14):5725–5733. doi:10.1021/jf0707637
Castillo MdP, Ander P, Stenström J, Torstensson L (2000) Degradation of the herbicide bentazon as related to enzyme production by Phanerochaete chrysosporium in two solid substrate fermentation systems. World J Microbiol Biotechnol 16(3):289–295. doi:10.1023/A:1008936617596
Castillo MdP, von Wirén-Lehr S, Scheunert I, Torstensson L (2001) Degradation of isoproturon by the white rot fungus Phanerochaete chrysosporium. Biol Fertil Soils 33(6):521–528. doi:10.1007/s003740100372
Castillo MdP, Torstensson L, Stenström J (2008) Biobeds for environmental protection from pesticide use—a review. J Agric Food Chem 56(15):6206–6219. doi:10.1021/jf800844x
Coppola L, Castillo MdP, Monaci E, Vischetti C (2007) Adaptation of the biobed composition for chlorpyrifos degradation to Southern Europe conditions. J Agric Food Chem 55(2):396–401. doi:10.1021/jf062744n
Cordeiro ML, Pompliano DL, Frost JW (1986) Degradation and detoxification of organophosphonates. Cleavage of the carbon-phosphorus bond. J Am Chem Soc 108(2):332–334. doi:10.1021/ja00262a044
Dick R, Quinn J (1995) Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Appl Microbiol Biotechnol 43(3):545–550. doi:10.1007/BF00218464
Duarte-Vázquez MA, Ortega-Tovar MA, García-Almendarez BE, Regalado C (2003) Removal of aqueous phenolic compounds from a model system by oxidative polymerization with turnip (Brassica napus L var purple top white globe) peroxidase. J Chem Technol Biotechnol 78(1):42–47. doi:10.1002/jctb.740
Eibes G, Lú-Chau T, Feijoo G, Moreira MT, Lema JM (2005) Complete degradation of anthracene by manganese peroxidase in organic solvent mixtures. Enzyme Microb Technol 37(4):365–372. doi:10.1016/j.enzmictec.2004.02.010
Faison BD, Kirk TK, Farrell RL (1986) Role of veratryl alcohol in regulating ligninase activity in Phanerochaete chrysosporium. Appl Environ Microbiol 52(2):251–254
Gianfreda L, Rao MA (2004) Potential of extra cellular enzymes in remediation of polluted soils: a review. Enzyme Microb Technol 35(4):339–354. doi:10.1016/j.enzmictec.2004.05.006
Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Annu Rev Microbiol 37:189–216. doi:10.1146/annurev.mi.37.100183.001201
Hammel K, Kalyanaraman B, Kirk T (1986) Oxidation of polycyclic aromatic hydrocarbons and dibenzo[p]-dioxins by Phanerochaete chrysosporium ligninase. J Biol Chem 261(36):16948–16952
Herpoël I, Asther M, Sigoillot J-C (1999) Design and scale up of a process for manganese peroxidase production using the hypersecretory strain Phanerochaete chrysosporium I-1512. Biotechnol Bioeng 65(4):468–473. doi:10.1002/(SICI)1097-0290(19991120)65:4<468::AID-BIT11>3.0.CO;2-J
Hirai H, Nakanishi S, Nishida T (2004) Oxidative dechlorination of methoxychlor by ligninolytic enzymes from white-rot fungi. Chemosphere 55(4):641–645. doi:10.1016/j.chemosphere.2003.11.035
Kapich A, Hofrichter M, Vares T, Hatakka A (1999) Coupling of manganese peroxidase-mediated lipid peroxidation with destruction of nonphenolic lignin model compounds and C-14-labeled lignins. Biochem Biophys Res Commun 259(1):212–219. doi:10.1006/bbrc.1999.0742
Kirk TK, Farrell RL (1987) Enzymatic “Combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41(1):465–501. doi:10.1146/annurev.mi.41.100187.002341
Kishore G, Jacob G (1987) Degradation of glyphosate by Pseudomonas sp. PG2982 via a sarcosine intermediate. J Biol Chem 262(25):12164–12168
Klimek M, Lejczak B, Kafarski P, Forlani G (2001) Metabolism of the phosphonate herbicide glyphosate by a non-nitrate-utilizing strain of Penicillium chrysogenum. Pest Manag Sci 57(9):815–821. doi:10.1002/ps.366
Kotterman MJJ, Vis EH, Field JA (1998) Successive mineralization and detoxification of benzo[a]pyrene by the white rot fungus Bjerkandera sp. strain BOS55 and indigenous microflora. Appl Environ Microbiol 64(8):2853–2858
Krzyśko-Lupicka T, Strof W, Kubś K, Skorupa M, Wieczorek P, Lejczak B, Kafarski P (1997) The ability of soil-borne fungi to degrade organophosphonate carbon-to-phosphorus bonds. Appl Microbiol Biotechnol 48(4):549–552. doi:10.1007/s002530051095
Liu C-M, McLean PA, Sookdeo CC, Cannon FC (1991) Degradation of the herbicide glyphosate by members of the family Rhizobiaceae. Appl Environ Microbiol 57(6):1799–1804
Mamy L, Barriuso E (2005) Glyphosate adsorption in soils compared to herbicides replaced with the introduction of glyphosate resistant crops. Chemosphere 61(6):844–855. doi:10.1016/j.chemosphere.2005.04.051
Mogadati PS, Louis JB, Rosen JD (1996) Determination of glyphosate and its metabolite (aminomethyl)phosphonic acid, in river water. J AOAC Int 79(1):157–162
Mohan SV, Prasad KK, Rao NC, Sarma PN (2005) Acid azo dye degradation by free and immobilized horseradish peroxidase (HRP) catalyzed process. Chemosphere 58(8):1097–1105. doi:10.1016/j.chemosphere.2004.09.070
Nüske J, Scheibner K, Dornberger U, Ullrich R, Hofrichter M (2002) Large scale production of manganese-peroxidase using agaric white-rot fungi. Enzyme Microb Technol 30(4):556–561. doi:10.1016/S0141-0229(02)00013-3
Obojska A, Ternan NG, Lejczak B, Kafarski P, McMullan G (2002) Organophosphonate utilization by the thermophile Geobacillus caldoxylosilyticus T20. Appl Environ Microbiol 68(4):2081–2084. doi:10.1128/AEM.68.4.2081-2084.2002
Park J-W, Park B-K, Kim J-E (2006) Remediation of soil contaminated with 2,4-dichlorophenol by treatment of minced shepherd’s purse roots. Arch Environ Contam Toxicol 50(2):191–195. doi:10.1007/s00244-004-0119-8
Paszczynski A, Crawford RL (1995) Potential for bioremediation of xenobiotic compounds by the white-rot fungus Phanerochaete chrysosporium. Biotechnol Prog 11(4):368–379. doi:10.1021/bp00034a002
Pipke R, Amrhein N (1988) Isolation and characterization of a mutant of Arthrobacter sp. strain GLP-1 which utilizes the herbicide glyphosate as its sole source of phosphorus and nitrogen. Appl Environ Microbiol 54(11):2868–2870
Pipke R, Amrhein N, Jacob GS, Schaefer J, Kishore GM (1987) Metabolism of glyphosate in an Arthrobacter sp. GLP-1. Eur J Biochem 165(2):267–273. doi:10.1111/j.1432-1033.1987.tb11437.x
Sims GK, Cupples AM (1999) Factors controlling degradation of pesticides in soil. Pestic Sci 55(5):598–601. doi:10.1002/(SICI)1096-9063(199905)55:5<598::AID-PS962>3.0.CO;2-N
Singh BK, Walker A (2006) Microbial degradation of organophosphorus compounds. FEMS Microbiol Rev 30(3):428–471. doi:10.1111/j.1574-6976.2006.00018.x
Srebotnik E, Boisson J-N (2005) Peroxidation of linoleic acid during the oxidation of phenols by fungal laccase. Enzyme Microb Technol 36(5–6):785–789. doi:10.1016/j.enzmictec.2005.01.004
Torstensson L (1985) Behaviour of glyphosate in soils and its degradation. In: Grossbard E, Atkinson D (eds) The herbicide glyphosate. Butterworths, London, pp 137–150
Torstensson L (1987) Microbial decomposition of herbicides in soil. In: Hutson DH, Roberts TR (eds) Herbicides. John Wiley & Sons, New York, pp 249–270
Trigo C, Ball AS (1994) Production of extracellular enzymes during the solubilisation of straw by Thermomonospora fusca BD25. Appl Microbiol Biotechnol 41(3):366–372. doi:10.1007/BF00221233
Tuncer M, Kuru A, Isikli M, Sahin N, Çelenk FG (2004) Optimization of extracellular endoxylanase, endoglucanase and peroxidase production by Streptomyces sp. F2621 isolated in Turkey. J Appl Microbiol 97(4):783–791. doi:10.1111/j.1365-2672.2004.02361.x
Wariishi H, Valli K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J Biol Chem 267(33):23688–23695
Wesenberg D, Kyriakides I, Agathos SN (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Prog 22(1–2):161–187
Zboinska E, Maliszewska I, Lejczak B, Kafarski P (1992) Degradation of organophosphonates by Penicillium citrinum. Lett Appl Microbiol 15(6):269–272. doi:10.1111/j.1472-765X.1992.tb00781.x
Acknowledgments
The authors thank Elisabet Börjesson (Department of Microbiology, SLU) for her technical help in the analyses of glyphosate and AMPA. This project was financed by the Centre for Chemical Pesticides (CKB) at SLU and by the Foundation for Strategic Environmental Research (MISTRA) by funding the research programme Domestication of Microorganisms (DOM).
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Pizzul, L., Castillo, M.d.P. & Stenström, J. Degradation of glyphosate and other pesticides by ligninolytic enzymes. Biodegradation 20, 751–759 (2009). https://doi.org/10.1007/s10532-009-9263-1
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DOI: https://doi.org/10.1007/s10532-009-9263-1