Interaction of Coal Humic Acids with Fungal Laccase

Natalia A. Kulikova, Valentina N. Davidchik, Eugenia A. Tsvetkova, Olga V. Koroleva

.
Department of Soil Science, M.V. Lomonosov Moscow State University, Moscow, Russia.

DOI: 10.4236/aim.2013.32023                

Abstract

Humic acids (HA) are one of the main environmental factors controlling the fate and behavior of the compounds released into the environment. In particular, they are universally considered of great importance in determining soil extracellular enzyme activity and stability via association with essential soil enzymes. The objective of this study was to investigate the interaction of coal HA with an extracellular multicopper oxidase laccase (EC 1.10.3.2) that catalyze the oxidation of a wide range of reducing substances in the environment. Using size-exclusion chromatography analysis and monitoring laccase activity, the formation of a stable and an enzymatically active complex between HA and laccase was shown. Basing the data obtained by isoelectric focusing of HA-laccase complex, non-covalent character of laccase association with HA was considered and binding of laccase to HA by weak dispersive forces such as van der Waals, hydrophobic, π-π, CH-π and others was hypothesized.

Keywords

Humic Acids; Laccase; Activity; Size-Exclusion Chromatography; Complexes; Isoelectric Focusing

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	E. M. Thurman, “Organic Geochemistry of Natural Waters,” Martinus Nijhof/Dr. W. Junk Publishers, Dordrecht, 1985.
[2]	D. S. Orlov, “Soil Humic Acids and General Theory of Humification”, Moscow State University Publisher, Moscow, 1990.
[3]	C. E. Clapp, M. H. B. Hayes and R. S. Swift, “Isolation, Fractionation, Functionalities, and Concepts of Structure of Soil Organic Macromolecules,” In: A. J. Beck, K. C. Jones, M. B. H. Hayes and U. Mingelgrin, Eds., Organic Substances in Soil and Water: Natural Constituents and Their Influence on Contaminant Behaviour, Royal Society of Chemistry, Cambridge, 1993, pp. 31-69.
[4]	G. Masciandaro and B. Ceccanti, “Assessing Soil Quality in Different Agro-Ecosystems through Biochemical and Chemico-Structural Properties of Humic Substances,” Soil and Tillage Research, Vol. 51, No. 1-2, 1999, pp. 129-137. doi:10.1016/S0167-1987(99)00056-2
[5]	E. Benitez, H. Sainz and R. Nogales, “Hydrolytic Enzyme Activities of Extracted Humic Substances during the Vermicomposting of a Lignocellulosic Olive Waste,” Bioresource Technology, Vol. 96, No. 7, 2005, pp. 785-790. doi:10.1016/j.biortech.2004.08.010
[6]	A. Messerschmidt, “Multi-Copper Oxidases,” World Scientific, Singapore, 1997.
[7]	F. Xu, “Recent Progress in Laccase Study: Properties, Enzymology, Production, and Applications,” In: M. C. Flickinger and S. W. Drew, Eds., Encyclopedia of Bioprocessing Technology: Fermentation, Biocatalysis, and Bioseparation, John Wiley & Sons, New York, 1999, pp. 1545-1554.
[8]	L. Gianfreda, F. Xu and J.-M. Bollag, “Laccases: A Useful Group of Oxidoreductive Enzymes,” Bioremediation Journal, Vol. 3, No. 1, 1999, pp. 1-25.
[9]	S. A. Gomes, J. M. Nogueira and M. J. Rebelo, “An Amperometric Biosensor for Polyphenolic Compounds in Red Wine,” Biosensors and Bioelectronics, Vol. 20, No. 6, 2004, pp. 1211-1216. doi:10.1016/j.bios.2004.05.013
[10]	T. Sonoki, S. Kajita, S. Ikeda, M. Uesugi, K. Tatsumi, Y. Katayama and Y. Iimura, “Transgenic Tobacco Expressing Fungal Laccase Promotes the Detoxification of Environmental Pollutants,” Applied Microbiology and Biotechnoogy, Vol. 67, No. 1, 2005, pp. 138-142. doi:10.1007/s00253-004-1770-8
[11]	R. Bourbonnais and M. G. Paice, “Enzymatic Delignification of Kraft Pulp Using Laccase and a Mediator,” Tappi Journal, Vol. 79, No. 6, 1996, pp. 199-204.
[12]	C. L. Crestini and D. S. Argyropoulos, “The Early Oxidative Biodegradation Steps of Residual Kraft Lignin Models with Laccase,” Bioorganic and Medicinal Chemistry, Vol. 6, No. 11, 1998, pp. 2161-2169. doi:10.1016/S0968-0896(98)00173-4
[13]	A. Ortega-Clemente, C. Estrada-Vazquez, F. Esparza-Garcia, S. Caffarel-Mendez, N. Rinderknecht-Seijas and H. M. Poggi-Varaldo, “Integrated Biological Treatment of Recalcitrant Effluents from Pulp Mills,” Water Science and Technology, Vol. 50, No. 3, 2004, pp. 145-156.
[14]	P. Schneider and A.H. Pedersen, “Enhancement of Laccase Reaction,” PCT International Patent WO 95/01426, European Patent Office, Munich, 1995.
[15]	R. C. Senan and T. E. Abraham, “Bioremediation of Textile Azo Dyes by Aerobic Bacterial Consortium—Aerobic Degradation of Selected Azo Dyes by Bacterial Consortium,” Biodegradation, Vol. 15, No. 4, 2004, pp. 275-280. doi:10.1023/B:BIOD.0000043000.18427.0a
[16]	S. Bohmer, K. Messner and E. Srebotnik, “Oxidation of Phenanthrene by a Fungal Laccase in the Presence of 1-hydroxybenzotriazole and Unsaturated Lipids,” Biochemical and Biophysical Research Communications, Vol. 244, No. 1,1998, pp. 233-238. doi:10.1006/bbrc.1998.8228
[17]	M. A. Pickard, R. Roman, R. Tinoco and R. VazquezDuhalt, “Polycyclic Aromatic Hydrocarbon Metabolism by White Rot Fungi and Oxidation by Coriolopsis gallica UAMH 8260 Laccase,” Applied and Environmental Microbiology, Vol. 65, No. 9, 1999, pp. 3805-3809.
[18]	C. Johannes, A. Majcherczyk and A. Hüttermann, “Degradation of Anthracene by Laccase of Trametes versicolor in the Presence of Different Mediator Compounds,” Applied Microbiology and Biotechnology, Vol. 46, No. 3, 1996, pp. 313-317.
[19]	A. Majcherczyk, C. Johannes and A. Hüttermann, “Oxidation of Polycyclic Aromatic Hydrocarbons (PAH) by Laccase of Trametes versicolor,” Enzyme and Microbial Technology, Vol. 22, No. 5, 1998, pp. 335-341. doi:10.1016/S0141-0229(97)00199-3
[20]	M. J. Han, H. T. Choi and H. G. Song, “Degradation of Phenanthrene by Trametes versicolor and Its Laccase,” Journal of Microbiology, Vol. 42, No. 2, 2004, pp. 94-98.
[21]	F. S. Sariaslani, J. M. Beale Jr. and P. Rosazza, “Oxidation of Rotenone by Polyporus anceps Laccase,” Journal of Natural Products, Vol. 47, No. 4, 1984, pp. 692-697.
[22]	G. Amitai, R. Adani, G. Sod-Moriah, I. Rabinovitz, A. Vincze, H. Leader, B. Chefetz, L. Leibovitz-Persky, D. Friesem and Y. Hadar, “Oxidative Biodegradation of Phosphorothiolates by Laccase,” FEBS Letters, Vol. 438, No. 3, 1998, pp. 195-200. doi:10.1016/S0014-5793(98)01300-3
[23]	S. Kawai, T. Umezawa and T. Higuchi, “Oxidation of Methoxylated Benzyl Alcohols by Laccase of Coriolus versicolor in the Presence of Syringaldehyde,” Wood Research, Vol. 76, 1989, pp. 10-16.
[24]	E. Fritz-Langhals and B. Kunath, “Synthesis of Aromatic Aldehydes by Laccase-Mediator Assisted Oxidation,” Tetrahedron Letters, Vol. 39, No. 33, 1998, pp. 5955-5956. doi:10.1016/S0040-4039(98)01215-5
[25]	A. Potthast, T. Rosenau, C. L. Chen and J. S. Gratzl, “A Novel Method for the Conversion of Benzyl Alcohols to Benzaldehydes by Laccase-Catalysed Oxidation,” Journal of Molecular Catalysis A: Chemical, Vol. 108, No. 1, 1996, pp. 5-9. doi:10.1016/1381-1169(95)00251-0
[26]	K.-H. Kang, J. Dec, H. Park and J.-M. Bollag, “Transformation of the Fungicide Cyprodinil by a Laccase of Trametes villosa in the Presence of Phenolic Mediators and Humic Acid,” Water Research, Vol. 36, No. 19, 2002, pp. 4907-4915. doi:10.1016/S0043-1354(02)00198-7
[27]	M.-Y. Ahn, J. Dec, J.-E. Kim and J.-M. Bollag, “Treatment of 2,4-dichlorophenol Polluted Soil with Free and Immobilized Laccase,” Journal of Environmental Quality, Vol. 31, No. 5, 2002, pp. 1509-1515.
[28]	R. M. Fakoussa and P. J. Frost, “In Vivo Decolorisation of Coal-Derived Humic Acids by Laccase Excreting Fungus Trametes versicolor,” Applied Microbiology Biotechnology, Vol. 52, No. 1, 1999, pp. 60-65.
[29]	Y.-S. Keum and Q. X. Li, “Copper Dissociation as Mechanism of Fungal Laccase Denaturation by Humic Acid,” Applied Microbiology and Biotechnology, Vol. 64, No. 4, 2004, pp. 588-592. doi:10.1007/s00253-003-1460-y
[30]	A. N. Kovalenko, M. V. Youdov, I. V. Perminova and V. S. Petrosyan, “Synthesis and Characterization of Humic Derivatives Enriched with Hydroquinoic and Catecholic Moieties,” Proceedings of the XII International Meeting of IHSS Humic Substances and Soil and Water Environment, Sao-Pedro, 25-30 July 2004, pp. 472-473.
[31]	O. V. Koroleva, E. V. Stepanova, V. P. Gavrilova, N. S. Yakovleva, E. O. Landesman, I. S. Yavmetdinov and A. I. Yaropolov, “Laccase and Mn-peroxidase Production by Coriolus hirsutus Strain 075 in a Jar Fermenter,” Journal of Bioscience and Bioengineering, Vol. 93, No. 5, 2002, pp. 449-455.
[32]	O. Koroleva (Skorobogat’ko), E. Stepanova, V. Gavrilova, O. Morozova, N. Lubimova, A. Dzchafarova, A. Yaropolov and A. Makower, “Purification and Characterization of the Constitutive Form of Laccase from the Basidiomycete Coriolus hirsutus and Effect of Inducers on Laccase Synthesis,” Biotechnology and Applied Biochemistry, Vol. 28, No. 1, 1998, pp. 47-54.
[33]	R. Westermeier, “Electrophoresis in Practice,” VCH Verlagsgesellschaft, Weinheim and VCH Publishers Inc., New York, 2001.
[34]	C. G. Kowalenko, L. J. P. van Vliet, G. Derksen and S. Yu, “Limitations of Methods for Preserving Ammonium in Agricultural Runoff Samples,” Canadian Journal of Soil Science, Vol. 82, No. 4, 2002, pp. 439-444.
[35]	I. V. Perminova, F. H. Frimmel, D. V. Kovalevskii, G. Abbt-Braun, A. V. Kudryavtsev and S. Hesse, “Development of a Predictive Model for Calculation of Molecular Weight of Humic Substances,” Water Research, Vol. 32, No. 3, 1998, pp. 872-881. doi:10.1016/S0043-1354(97)00283-2
[36]	A. V. Kudryavtsev, I. V. Perminova and V. S. Petrosyan, “Size-exclusion Chromatographic Descriptors of Humic Substances,” Analytica Chimica Acta, Vol. 407, No. 1-2, 2000, pp. 193-202. doi:10.1016/S0003-2670(99)00814-4
[37]	P. G. Righetti, “Isoelectric Focusing: Theory, Methodology and Applications,” Elsevier Biomedical Press, Amsterdam, 1983.
[38]	I. V. Perminova, “Size-exclusion Chromatography of Humic Substances: Complexities of Data Interpretation Attributable to Non-size Exclusion Effects,” Soil Science, Vol. 164, No. 11, 1999, pp. 834-840. doi:10.1097/00010694-199911000-00008
[39]	O. V. Koroleva (Skorobogat’ko), E. V. Stepanova, V. P. Gavrilova, V. I. Biniukov, A. I. Jaropolov, S. D. Varfolomeyev, F. Scheller, A. Makower and A. Otto, “Laccase of Coriolus zonatus Isolation, Purification and Some Physico-Chemical Properties,” Biotechnology and Applied Biochemistry, Vol. 76, No. 2, 1999, pp. 115-127.
[40]	A. Cozzolino and A. Piccolo, “Polymerization of Dissolved Humic Substances Catalyzed by Peroxidase. Effects of pH and Humic Composition,” Organic Geochemistry, Vol. 33, No. 3, 2002, pp. 281-294. doi:10.1016/S0146-6380(01)00160-7
[41]	S. H. Van Erp, E. O. Kamenskaya and Y. L. Khmelnitsky, “The Effect of Water Content and Nature of Organic Solvent on Enzyme Activity in Low-Water Media. A Quantitative Description,” European Journal of Biochemistry, Vol. 202, No. 2, 1991, pp. 379-384. doi:10.1111/j.1432-1033.1991.tb16385.x
[42]	J. Rodakiewicz-Nowak, J. Haber, N. Pozdnyakova, A. Leontievsky and L. A. Golovleva, “Effect of Ethanol on Enzymatic Activity of Fungal Laccases,” Bioscience Reports, Vol. 19, No. 6, 1999, pp. 589-600. doi:10.1023/A:1020223130115
[43]	J. Rodakiewicz-Nowak, “Phenols Oxidizing Enzymes in Water-Restricted Media,” Topics in Catalysis, Vol. 11-12, No. 1-4, 2000, pp. 419-434. doi:10.1023/A:1027291629302
[44]	U. Temp, H. Meyrahn and C. Eggert, “Extracellular Phenol Oxidase Pattern during Depolymerization of Low-Rank Coal by Three Basidiomycetes,” Biotechnology Letters, Vol. 21, No. 4, 1999, pp. 281-287. doi:10.1023/A:1005491818192
[45]	R. McMillin and M. K. Eggleston, “Bioinorganic Chemistry of Laccase,” In: Messerschmidt, Ed., Multicopper Oxidases, World Scientific, Singapore, New Jersey, London, Hong Kong, 1997, pp. 129-166.
[46]	O. V. Koroleva, E. V. Stepanova, V. P. Gavrilova, V. I. Biniukov and A. M. Pronin, “Comparative Characterization of Methods for Removal of Cu(II) from the Active Sites of Fungal Laccases,” Biochemistry-Moscow, Vol. 66, No. 9, 2001, pp. 960-966. doi:10.1023/A:1012357223083