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Biology and Fertility of Soils

, Volume 50, Issue 7, pp 1015–1024 | Cite as

Enhanced non-extractable residue formation of 14C-metalaxyl catalyzed by an immobilized laccase

  • Jens Botterweck
  • Burkhard Schmidt
  • Jan Schwarzbauer
  • Roschni Kalathoor
  • Andreas Schäffer
Original Paper

Abstract

We studied the influence of an immobilized laccase from Trametes versicolor on non-extractable residue (NER) formation of the systemic fungicide 14C-metalaxyl in soil. We added the enzyme (130 mU/g DW) to soil sterilized by gamma irradiation and observed that the amount of NER (6.3 % of applied radioactivity) after 10 days of incubation was enhanced about twofold compared to the sterile soil without laccase addition. Residues formed within samples without enhanced enzyme activity were mainly bound via ester linkages to all fractions of humic matter, i.e., fulvic acids, humic acids, non-humines, and humines, respectively. In contrast, residues formed in presence of immobilized laccase were more strongly bound by covalent linkages such as ether and C-C bonds, especially to humic acids. After chemical degradation of the humic matter, it could be observed that all NER contained the first major transformation product, i.e., metalaxyl acid. The findings underline that the residue formation of metalaxyl in soil may be partly catalyzed by immobilized extracellular oxidative enzymes through oxidative coupling reactions within the humic matter.

Keywords

Non-extractable residues Immobilized soil enzymes Metalaxyl Laccase 

Notes

Acknowledgments

We wish to thank the German Research Foundation (DFG) for funding of the research unit (SPP1315: Biogeochemical interfaces in soil.

References

  1. Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2(1):1–12. doi: 10.2478/v10102-009-0001-7 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Alef K, Kleiner D (1989) Rapid and sensitive determination of microbial activity in soils and in soil aggregates by dimethylsulfoxide reduction. Biol Fertil Soils 8:349–355CrossRefGoogle Scholar
  3. Baker KL, Marshall S, Nicol GW, Campbell CD, Nicollier C, Ricketts D, Kilham K, Prosser JI (2010) Degradation of metalaxyl-M in contrasting soils is influenced more by differences in physicochemical characteristics than in microbial community composition after re-inoculation of sterilised soils. Soil Biol Biochem 42:1123–1131CrossRefGoogle Scholar
  4. Barraclough D, Kearney T, Croxford A (2005) Bound residues: environmental solution or future problem? Environ Pollut 133:85–90PubMedCrossRefGoogle Scholar
  5. Barriuso E, Benoit P, Dubus IG (2008) Formation of pesticide nonextractable (bound) residues in soil: magnitude, controlling factors and reversibility. Environ Sci Technol 42:1845–1854PubMedCrossRefGoogle Scholar
  6. Berns AE, Bertmer M, Schäffer A, Meyer RJ, Vereecken H, Lewandowski H (2007) The 15N-CPMAS NMR spectra of simazine and its metabolites—measurements and quantum chemical calculations. Eur J Soil Sci 58:882–888CrossRefGoogle Scholar
  7. Bollag JM (1983) Cross coupling of humus constituents and xenobiotic substances. In: Christman RF, Gjessing ET (Eds) Aquatic and terrestrial humic material. Ann. Arbor Science, Ann Arbor, Michigan, 127–141Google Scholar
  8. Bollag JM, Sjoblad RD, Minard RD (1977) Polymerization of phenolic intermediates of pesticides by fungal enzyme. Experientia 33:1564–1566PubMedCrossRefGoogle Scholar
  9. Bollag JM, Liu SY, Minard RD (1980) Cross-coupling of phenolic humus constituents and 2,4-dichlorophenol. Soil Sci Soc Am J 44:52–56CrossRefGoogle Scholar
  10. Bollag JM, Myers CJ, Minard RD (1992) Biological and chemical interactions of pesticides with soil organic matter. Sci Total Environ 123/124:205–217CrossRefGoogle Scholar
  11. Botterweck J, Claßen D, Zegarski T, Gottfroh C, Kalathoor R, Schäffer A, Schwarzbauer J, Schmidt B (2014) A correlation between the fate and non-extractable residue formation of 14C-metalaxyl and enzymatic activities in soil. Environ Sci Health B 49(2):69–78CrossRefGoogle Scholar
  12. Burns RG (1982) Enzyme activity in soil: location and possible role in microbial ecology. Soil Biol Biochem 14:423–427CrossRefGoogle Scholar
  13. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein ME, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  14. Duran N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99CrossRefGoogle Scholar
  15. Duran N, Rosa MA, Annibale AD, Gianfreda L (2002) Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzym Microb Technol 31:907–931CrossRefGoogle Scholar
  16. Fernandes MC, Cox L, Hermosin MC, Cornjeo J (2003) Adsorption-desorption of metalaxyl as affecting dissipation and leaching in soils: role of mineral and organic components. Pest Manag Sci 59(545):552Google Scholar
  17. Floch C, Alarcon-Guierrez E, Criquet S (2007) ABTS assay of phenol oxidase activity in soil. J Microbiol Methods 71:319–324PubMedCrossRefGoogle Scholar
  18. Gerzabek MH, Antil RS, Kögel-Knabner I, Knicker H, Kirchmann H, Haberhauer G (2006) How are soil use and management reflected by soil organic matter characteristics: a spectroscopic approach. Eur J Soil Sci 52:485–494CrossRefGoogle Scholar
  19. Gevao B, Semple KT, Jones KC (2000) Bound pesticide residues in soil: a review. Environ Pollut 108:3–14PubMedCrossRefGoogle Scholar
  20. Gianfreada L, Rao MA (2004) Potential of extracellular enzymes in remediation of polluted soils: a review. Enzym Microb Technol 35:339–354CrossRefGoogle Scholar
  21. Gianfreda L, Bollag JM (1994) Effect of soils on the behaviour of immobilized enzymes. Soil Sci Soc Am J 58:1672–1681CrossRefGoogle Scholar
  22. Gulkowska A, Sander M, Hollender J, Krauss M (2013) Covalent binding of sulfamethazine to natural and synthetic humic acids: assessing laccase catalysis and covalent bond stability. Environ Sci Technol 47:6916–6924PubMedGoogle Scholar
  23. Haider K, Spiteller M, Dec J, Schäffer A (2000) Silylation of organic matter: extraction of humic compounds and soil-bound residues. In: Bollag JM, Stotzky G (eds) Soil biochemistry, vol 10. Marcel Dekker Verlag, New York, pp 139–170Google Scholar
  24. Karam J, Nicell JA (1997) Potential application of enzymes in waste treatment. J Chem Technol Biotechnol 69:141–153CrossRefGoogle Scholar
  25. Kästner M, Nowak KM, Miltner A, Trapp S, Schäffer A (2013) Classification and modelling of non-extractable residue (NER) formation of xenobiotics in soil—a synthesis. Crit Rev Environ Sci Technol. doi: 10.1080/10643389.2013.828270 Google Scholar
  26. Kirchmann H, Persson J, Carlgren K (1994) The Ultuna long-term soil organic matter experiment, 1956–91. Reports and Dissertations 17, Department of Soil Science, Swedish University of Agricultural Sciences, UppsalaGoogle Scholar
  27. Kohl SD, Rice JA (1998) The binding of contaminants to humin: a mass balance. Chemosphere 36:251–261CrossRefGoogle Scholar
  28. Monkiedje A, Ilori MO, Spiteller M (2002) Soil quality changes resulting from the application of the fungicides mefenoxam and metalaxyl to a sandy loam soil. Soil Biol Biochem 34:1939–1948CrossRefGoogle Scholar
  29. Mordaunt CJ, Gevao B, Jones KC, Semple KT (2005) Formation of non-extractable pesticide residues: observations on compound differences, measurement and regulatory issues. Environ Pollut 133:25–34PubMedCrossRefGoogle Scholar
  30. Nannipieri P, Bollag JM (1991) Use of enzymes to detoxify pesticide-contaminated soils and waters. J Environ Qual 20:510–570Google Scholar
  31. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762CrossRefGoogle Scholar
  32. Nicell JA (2001) Environmental applications of enzymes. Interdiscip Environ Rev 3:14–41CrossRefGoogle Scholar
  33. Nowak K, Miltner A, Gehre M, Schäffer A, Kästner M (2011) Formation and fate of “bound” residues from microbial biomass during biodegradation of 2,4-D in soil. Environ Sci Technol 45:1127–1132CrossRefGoogle Scholar
  34. Palmieri G, Giardina P, Desiderio B, Marzulla L, Giamberini M, Sannia G (1994) A new immobilization procedure using copper alginate gel: application to a fungal phenol oxidase. Enzym Microb Technol 16:151–158CrossRefGoogle Scholar
  35. Pesaro M, Nicollier G, Zeyer J, Widmer F (2004) Impact of soil drying-rewetting stress on microbial communities and activities and on degradation of two crop protection products. Appl Environ Microbiol 70(5):2577–2587PubMedPubMedCentralCrossRefGoogle Scholar
  36. Riefer J, Klausmayer T, Schwarzbauer J, Schäffer A, Schmidt B, Corvini PFX (2010) Rapid incorporation and short-term distribution of a nonylphenol isomer and the herbicide MCPA in soil-derived organo-clay complexes. Environ Chem Lett 903:411–415Google Scholar
  37. Rodriguez-Cruz MS, Andrades MJ, Sanchez-Martin MJ (2008) Significance of the long-chain organic cation structure in the sorption of the penconazole and metalaxyl fungicides by organo clays. J Hazard Chem 160:200–207CrossRefGoogle Scholar
  38. Senesi N (1992) Binding mechanisms of pesticides to soil humic substances. Sci Total Environ 123/124:63–76CrossRefGoogle Scholar
  39. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  40. Stemmer M, Gerzabek MH, Kandeler E (1998) Organic matter and enzyme activity in particle-size fractions of soils obtained after low-energy sonication. Soil Biol Biochem 30:9–17CrossRefGoogle Scholar
  41. Sukul P, Spiteller M (2001) Persistence, fate and metabolism of 14C-metalaxyl in typical Indian soils. J Agric Food Chem 49:2352–2358PubMedCrossRefGoogle Scholar
  42. Sukul P, Moza PN, Hustert K, Kettrup A (1992) Photochemistry of metalaxyl. J Agric Food Chem 40:2488–2492CrossRefGoogle Scholar
  43. Sukul P, Lamshöft M, Zühlke S, Spiteller M (2013) Evaluation of sorption–desorption processes for metalaxyl in natural and artificial soils. J Environ Sci Health B 48:431–441PubMedCrossRefGoogle Scholar
  44. Totsche KU, Rennert T, Gerzabek M, Kögel-Knabner I, Smalla K, Spiteller M, Vogel HJ (2010) Biogeochemical interfaces in soil: the interdisciplinary challenge for soil science. J Plant Nutr Soil Sci 173:88–99CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Jens Botterweck
    • 1
  • Burkhard Schmidt
    • 1
  • Jan Schwarzbauer
    • 2
  • Roschni Kalathoor
    • 2
  • Andreas Schäffer
    • 1
  1. 1.Institute for Environmental ResearchRWTH Aachen UniversityAachenGermany
  2. 2.Institute of Petroleum & Coal, Structural GeologyEMR RWTH Aachen UniversityAachenGermany

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