Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Alef K, Kleiner D (1989) Rapid and sensitive determination of microbial activity in soils and in soil aggregates by dimethylsulfoxide reduction. Biol Fertil Soils 8:349–355

    Article  CAS  Google Scholar 

  • 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 42:1123–1131

    Article  CAS  Google Scholar 

  • Barraclough D, Kearney T, Croxford A (2005) Bound residues: environmental solution or future problem? Environ Pollut 133:85–90

    Article  PubMed  CAS  Google Scholar 

  • Barriuso E, Benoit P, Dubus IG (2008) Formation of pesticide nonextractable (bound) residues in soil: magnitude, controlling factors and reversibility. Environ Sci Technol 42:1845–1854

    Article  PubMed  CAS  Google Scholar 

  • 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 58:882–888

    Article  CAS  Google Scholar 

  • 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, 127–141

  • Bollag JM, Sjoblad RD, Minard RD (1977) Polymerization of phenolic intermediates of pesticides by fungal enzyme. Experientia 33:1564–1566

    Article  PubMed  CAS  Google Scholar 

  • Bollag JM, Liu SY, Minard RD (1980) Cross-coupling of phenolic humus constituents and 2,4-dichlorophenol. Soil Sci Soc Am J 44:52–56

    Article  CAS  Google Scholar 

  • Bollag JM, Myers CJ, Minard RD (1992) Biological and chemical interactions of pesticides with soil organic matter. Sci Total Environ 123/124:205–217

    Article  Google Scholar 

  • 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):69–78

    Article  CAS  Google Scholar 

  • Burns RG (1982) Enzyme activity in soil: location and possible role in microbial ecology. Soil Biol Biochem 14:423–427

    Article  CAS  Google Scholar 

  • 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 58:216–234

    Article  CAS  Google Scholar 

  • 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 28:83–99

    Article  CAS  Google Scholar 

  • Duran N, Rosa MA, Annibale AD, Gianfreda L (2002) Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzym Microb Technol 31:907–931

    Article  CAS  Google Scholar 

  • 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):552

    Google Scholar 

  • Floch C, Alarcon-Guierrez E, Criquet S (2007) ABTS assay of phenol oxidase activity in soil. J Microbiol Methods 71:319–324

    Article  PubMed  CAS  Google Scholar 

  • 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 52:485–494

    Article  Google Scholar 

  • Gevao B, Semple KT, Jones KC (2000) Bound pesticide residues in soil: a review. Environ Pollut 108:3–14

    Article  PubMed  CAS  Google Scholar 

  • Gianfreada L, Rao MA (2004) Potential of extracellular enzymes in remediation of polluted soils: a review. Enzym Microb Technol 35:339–354

    Article  Google Scholar 

  • Gianfreda L, Bollag JM (1994) Effect of soils on the behaviour of immobilized enzymes. Soil Sci Soc Am J 58:1672–1681

    Article  CAS  Google Scholar 

  • 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 47:6916–6924

    PubMed  CAS  Google Scholar 

  • 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 139–170

    Google Scholar 

  • Karam J, Nicell JA (1997) Potential application of enzymes in waste treatment. J Chem Technol Biotechnol 69:141–153

    Article  CAS  Google Scholar 

  • 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 

  • 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, Uppsala

  • Kohl SD, Rice JA (1998) The binding of contaminants to humin: a mass balance. Chemosphere 36:251–261

    Article  CAS  Google Scholar 

  • 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 34:1939–1948

    Article  CAS  Google Scholar 

  • 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 133:25–34

    Article  PubMed  CAS  Google Scholar 

  • Nannipieri P, Bollag JM (1991) Use of enzymes to detoxify pesticide-contaminated soils and waters. J Environ Qual 20:510–570

  • 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 48:743–762

    Article  Google Scholar 

  • Nicell JA (2001) Environmental applications of enzymes. Interdiscip Environ Rev 3:14–41

    Article  Google Scholar 

  • 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 45:1127–1132

    Article  Google Scholar 

  • 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 16:151–158

    Article  CAS  Google Scholar 

  • 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):2577–2587

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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 903:411–415

    Google Scholar 

  • 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 160:200–207

    Article  CAS  Google Scholar 

  • Senesi N (1992) Binding mechanisms of pesticides to soil humic substances. Sci Total Environ 123/124:63–76

    Article  Google Scholar 

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • 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 30:9–17

    Article  CAS  Google Scholar 

  • Sukul P, Spiteller M (2001) Persistence, fate and metabolism of 14C-metalaxyl in typical Indian soils. J Agric Food Chem 49:2352–2358

    Article  PubMed  CAS  Google Scholar 

  • Sukul P, Moza PN, Hustert K, Kettrup A (1992) Photochemistry of metalaxyl. J Agric Food Chem 40:2488–2492

    Article  CAS  Google Scholar 

  • 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 48:431–441

    Article  PubMed  CAS  Google Scholar 

  • 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 173:88–99

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

  1. Institute for Environmental Research, RWTH Aachen University, Worringerweg 1, 52074, Aachen, Germany

    Jens Botterweck, Burkhard Schmidt & Andreas Schäffer

  2. Institute of Petroleum & Coal, Structural Geology, EMR RWTH Aachen University, Aachen, Germany

    Jan Schwarzbauer & Roschni Kalathoor

Authors
  1. Jens Botterweck
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Burkhard Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jan Schwarzbauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roschni Kalathoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andreas Schäffer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jens Botterweck.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Botterweck, J., Schmidt, B., Schwarzbauer, J. et al. Enhanced non-extractable residue formation of 14C-metalaxyl catalyzed by an immobilized laccase. Biol Fertil Soils 50, 1015–1024 (2014). https://doi.org/10.1007/s00374-014-0923-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-014-0923-x

Keywords

Search

Navigation