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Phenolic Compound Biotransformation by Trametes versicolor ATCC 200801 and Molecular Docking Studies

  • João Carlos Silva Conceição
  • Herbert Júnior Dias
  • Clarissa Maria Souza Peralva
  • Antônio Eduardo Miller Crotti
  • Samuel Silva da Rocha Pita
  • Eliane de Oliveira SilvaEmail author
Article

Abstract

The filamentous fungus Trametes versicolor is a rich source of laccase (Tvlac). Laccases catalyze reactions that convert substituted phenol substrates into diverse derivatives through aromatic oxidation. We investigated methyl p-coumarate, methyl ferulate, and methyl caffeate biotransformation by Trametes versicolor ATCC 200801. Despite substrate similarity, the biotransformation reactions varied widely. Only methyl p-coumarate was converted into three derivatives. We isolated and identified the chemical structures of such derivatives by NMR and IR analysis. Hydroxylation, methylation, and hydrolysis were the main reactions resulting from the studied biotransformation. We also analyzed the interactions between Tvlac (PDB ID: 1GYC) and the three phenolic substrates by molecular docking simulations. The substituents in the phenol ring influenced substrate conformation and orientation in the Tvlac site. The biotransformation reaction selectivity correlated with the different binding energies to the Tvlac site. Our results demonstrated that docking studies successfully predict the biotransformation of cinnamic acid analogs by T. versicolor.

Keywords

Biotransformation Laccase Molecular docking Phenolic compounds Trametes versicolor 

Notes

Acknowledgments

JCSC thanks FAPESB for his scholarship.

Funding Information

This work was supported by the Brazilian National Council for Scientific and Technological Development (CNPq), Brazilian Coordination for Improvement of Personnel Higher Education (CAPES), and Bahia Research Foundation (FAPESB, grant numbers JCB-0039/2013 and RED-008/2013).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

12010_2019_3191_MOESM1_ESM.docx (528 kb)
ESM 1 (DOCX 527 kb)

References

  1. 1.
    Lenardão, E. J., Freitag, R. A., Dabdoub, M. J., Batista, A. C. F., & da C Silveira, C. (2003). “Green chemistry”: os 12 princípios da química verde e sua inserção nas atividades de ensino e pesquisa. Química Nova, 26(1), 123–129.  https://doi.org/10.1590/S0100-40422003000100020.CrossRefGoogle Scholar
  2. 2.
    Hai-Feng, Z., Guo-Qing, H., Jing, L., Hui, R., Qi-He, C., Qiang, Z., & Hong-Bo, Z. (2008). Production of gastrodin through biotransformation of p-2-hydroxybenzyl alcohol by cultured cells of Armillaria luteo-virens Sacc. Enzyme and Microbial Technology, 43, 25–30.  https://doi.org/10.1016/j.enzmictec.2008.03.007.CrossRefGoogle Scholar
  3. 3.
    Rivera-Hoyos, C. M., Morales-Alvarez, E. D., Pedroza-Rodríguez, A. M., Rodríguez-Vásquez, R., & Delgado-Boada, J. M. (2013). Fungal laccases. Fungal Biology Reviews, 27, 67–82.  https://doi.org/10.1016/j.fbr.2013.07.001.CrossRefGoogle Scholar
  4. 4.
    Margot, J., Bennati-Granier, C., Maillard, J., Blánquez, P., Barry, D. A., & Holliger, C. (2013). Bacterial versus fungal laccase: potential for micropollutant degradation. AMB Express, 3(1), 63.  https://doi.org/10.1186/2191-0855-3-63.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Heinzkill, M., Bech, L., Halkier, T., Schneider, P., & Anke, T. (1998). Characterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae). Applied and Environmental Microbiology, 64, 1601–16056.PubMedPubMedCentralGoogle Scholar
  6. 6.
    Caparrós-Ruiz, D., Fornalé, S., Civardi, L., Puigdomènech, P., & Rigau, J. (2006). Isolation and characterisation of a family of laccases in maize. Plant Science, 171(2), 217–225.  https://doi.org/10.1016/j.plantsci.2006.03.007.CrossRefGoogle Scholar
  7. 7.
    Ullah, M. A., Bedford, C. T., & Evans, C. S. (2000). Reactions of pentachlorophenol with laccase from Coriolus versicolor. Applied Microbiology and Biotechnology, 53(2), 230–234.  https://doi.org/10.1007/s002530050013.CrossRefPubMedGoogle Scholar
  8. 8.
    Abadulla, E., Tzanov, T., Costa, S., Robra, K.-H., Cavaco-Paulo, A., & Gubitz, G. M. (2000). Decolorization and detoxification of textile dyes with a laccase from Trametes hirsuta. Applied and Environmental Microbiology, 66(8), 3357–3362.  https://doi.org/10.1128/AEM.66.8.3357-3362.2000.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Riva, S. (2006). Laccases: blue enzymes for green chemistry. Trends in Biotechnology, 24(5), 219–226.  https://doi.org/10.1016/j.tibtech.2006.03.006.CrossRefPubMedGoogle Scholar
  10. 10.
    Baldrian, P. (2006). Fungal laccases – occurrence and properties. FEMS Microbiology Reviews, 30(2), 215–242.  https://doi.org/10.1111/j.1574-4976.2005.00010.x.CrossRefPubMedGoogle Scholar
  11. 11.
    Wang, F., Hu, J.-H., Guo, C., & Liu, C.-Z. (2014). Enhanced laccase production by Trametes versicolor using corn steep liquor as both nitrogen source and inducer. Bioresource Technology, 166, 602–605.  https://doi.org/10.1016/j.biortech.2014.05.068.CrossRefPubMedGoogle Scholar
  12. 12.
    Iimura, Y., Sonoki, T., & Habe, H. (2018). Heterologous expression of Trametes versicolor laccase in Saccharomyces cerevisiae. Protein Expression and Purification, 141, 39–43.  https://doi.org/10.1016/j.pep.2017.09.004.CrossRefPubMedGoogle Scholar
  13. 13.
    Martínez-Sotres, C., Rutiaga-Quiñones, J. G., Herrera-Bucio, R., Gallo, M., & López-Albarrán, P. (2015). Molecular docking insights into the inhibition of laccase activity by medicarpin. Wood Science and Technology, 49(4), 857–868.  https://doi.org/10.1007/s00226-015-0734-8.CrossRefGoogle Scholar
  14. 14.
    Kameshwar, A. K. S., Barber, R., & Qin, W. (2018). Comparative modeling and molecular docking analysis of white, brown and soft rot fungal laccases using lignin model compounds for understanding the structural and functional properties of laccases. Journal of Molecular Graphics and Modelling, 79, 15–26.  https://doi.org/10.1016/j.jmgm.2017.10.019.CrossRefPubMedGoogle Scholar
  15. 15.
    Mikolasch, A., Matthies, A., Lalk, M., & Schauer, F. (2008). Laccase-induced C–-N coupling of substituted p-hydroquinones with p-aminobenzoic acid in comparison with known chemical routes. Applied Microbiology and Biotechnology, 80(3), 389–397.  https://doi.org/10.1007/s00253-008-1595-y.CrossRefPubMedGoogle Scholar
  16. 16.
    de Oliveira Silva, E., & Batista, R. (2017). Ferulic acid and naturally occurring compounds bearing a feruloyl moiety: a review on their structures, occurrence, and potential health benefits. Comprehensive Reviews in Food Science and Food Safety, 16, 580–616.  https://doi.org/10.1111/1541-4337.12266.CrossRefGoogle Scholar
  17. 17.
    Stoilova, I., Krastanov, A., & Stanchev, V. (2010). Properties of crude laccase from Trametes versicolor produced by solid-substrate fermentation. Advances in Bioscience and Biotechnology, 01, 208–215.  https://doi.org/10.4236/abb.2010.13029.CrossRefGoogle Scholar
  18. 18.
    Witayakran, S., & Ragauskas, A. J. (2009). Synthetic applications of laccase in Green Chemistry. Advanced Synthesis & Catalysis, 351, 1187–1209.  https://doi.org/10.1002/adsc.200800775.CrossRefGoogle Scholar
  19. 19.
    Trejo-Hernandez, M. R., Lopez-Munguia, A., & Quintero Ramirez, R. (2001). Residual compost of Agaricus bisporus as a source of crude laccase for enzymic oxidation of phenolic compounds. Process Biochemistry, 36, 635–639.  https://doi.org/10.1016/S0032-9592(00)00257-0.CrossRefGoogle Scholar
  20. 20.
    Falconnier, B., Lapierre, C., Lesage-Meessen, L., Yonnet, G., Brunerie, P., Colonna-Ceccaldi, B., & Asther, M. (1994). Vanillin as a product of ferulic acid biotransformation by the white-rot fungus Pycnoporus cinnabarinus I-937: identification of metabolic pathways. Journal of Biotechnology, 37, 123–132.  https://doi.org/10.1016/0168-1656(94)90003-5.CrossRefGoogle Scholar
  21. 21.
    Boaventura, M. A. D., Lopes, R. F. A. P., & Takahashi, J. A. (2004). Microorganisms as tools in modern chemistry: the biotransformation of 3-indolylacetonitrile and tryptamine by fungi. Brazilian Journal of Microbiology, 35, 345–347.CrossRefGoogle Scholar
  22. 22.
    Garzón-Posse, F., Becerra-Figueroa, L., Hernández-Arias, J., & Gamba-Sánchez, D. (2018). Whole cells as biocatalysts in organic transformations. Molecules, 23(6), 1265.  https://doi.org/10.3390/molecules23061265.CrossRefPubMedCentralGoogle Scholar
  23. 23.
    de Carvalho, C. C. C. R. (2017). Whole cell biocatalysts: essential workers from Nature to the industry. Microbial Biotechnology, 10(2), 250–263.  https://doi.org/10.1111/1751-7915.12363.CrossRefPubMedGoogle Scholar
  24. 24.
    Höring, P., Rothschild-Mancinelli, K., Sharma, N. D., Boyd, D. R., & Allen, C. C. R. (2016). Oxidative biotransformations of phenol substrates catalysed by toluene dioxygenase: a molecular docking study. Journal of Molecular Catalysis B: Enzymatic, 134, 396–406.  https://doi.org/10.1016/j.molcatb.2016.10.013.CrossRefGoogle Scholar
  25. 25.
    Awasthi, M., Jaiswal, N., Singh, S., Pandey, V. P., & Dwivedi, U. N. (2015). Molecular docking and dynamics simulation analyses unraveling the differential enzymatic catalysis by plant and fungal laccases with respect to lignin biosynthesis and degradation. Journal of Biomolecular Structure and Dynamics, 33, 1835–1849.  https://doi.org/10.1080/07391102.2014.975282.CrossRefPubMedGoogle Scholar
  26. 26.
    Mo, D., Zeng, G., Yuan, X., Chen, M., Hu, L., Li, H., & Cheng, M. (2018). Molecular docking simulation on the interactions of laccase from Trametes versicolor with nonylphenol and octylphenol isomers. Bioprocess and Biosystems Engineering, 41(3), 331–343.  https://doi.org/10.1007/s00449-017-1866-z.CrossRefPubMedGoogle Scholar
  27. 27.
    Hongyan, L., Zexiong, Z., Shiwei, X., He, X., Yinian, Z., Haiyun, L., & Zhongsheng, Y. (2019). Study on transformation and degradation of bisphenol A by Trametes versicolor laccase and simulation of molecular docking. Chemosphere, 224, 743–750.  https://doi.org/10.1016/j.chemosphere.2019.02.143.CrossRefPubMedGoogle Scholar
  28. 28.
    Pieters, L., Van Dyck, S., Gao, M., Bai, R., Hamel, E., Vlietinck, A., & Lemière, G. (1999). Synthesis and biological evaluation of dihydrobenzofuran lignans and related compounds as potential antitumor agents that inhibit tubulin polymerization. Journal of Medicinal Chemistry, 42, 5475–5481.  https://doi.org/10.1021/jm990251m.CrossRefPubMedGoogle Scholar
  29. 29.
    Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791.  https://doi.org/10.1002/jcc.21256.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Rodrigues, R. P., Mantoani, S. P., de Almeida, J. R., Pinsetta, F. R., Semighini, E. P., da Silva, V. B., & Silva, C. H. T. P. (2012). Virtual screening strategies in drug design. Revista Virtual de Química, 4, 739–776.  https://doi.org/10.5935/1984-6835.20120055.CrossRefGoogle Scholar
  31. 31.
    da Paixão, V. G., & da R Pita, S. S. (2019). In silico identification and evaluation of new Trypanosoma cruzi trypanothione reductase (TcTR) inhibitors obtained from natural products database of the Bahia semi-arid region (NatProDB). Computational Biology and Chemistry, 79, 36–47.  https://doi.org/10.1016/j.compbiolchem.2019.01.009.CrossRefPubMedGoogle Scholar
  32. 32.
    Huey, R., Morris, G. M., Olson, A. J., & Goodsell, D. S. (2007). A semiempirical free energy force field with charge-based desolvation. Journal of Computational Chemistry, 28(6), 1145–1152.  https://doi.org/10.1002/jcc.20634.CrossRefPubMedGoogle Scholar
  33. 33.
    Gasteiger, J., & Marsili, M. (1980). Iterative partial equalization of orbital electronegativity-a rapid access to atomic charges. Tetrahedron, 36, 3219–3228.  https://doi.org/10.1016/0040-4020(80)80168-2.CrossRefGoogle Scholar
  34. 34.
    Montanari, C. (2011). Química Medicinal: métodos e fundamentos em planejamento de fármacos (1st ed.). São Paulo: EDUSP.Google Scholar
  35. 35.
    Salameh, D., Brandam, C., Medawar, W., Lteif, R., & Strehaiano, P. (2008). Highlight on the problems generated by p-coumaric acid analysis in wine fermentations. Food Chemistry, 107, 1661–1667.  https://doi.org/10.1016/j.foodchem.2007.09.052.CrossRefGoogle Scholar
  36. 36.
    Foti, M. C., Daquino, C., & Geraci, C. (2004). Electron-transfer reaction of cinnamic acids and their methyl esters with the DPPH radical in alcoholic solutions. The Journal of Organic Chemistry, 69, 2309–2314.  https://doi.org/10.1021/jo035758q.CrossRefPubMedGoogle Scholar
  37. 37.
    Li, Y., & Hesse, M. (2003). The syntheses of cyclic spermine alkaloids: analogues of buchnerine and budmunchiamine C. Helvetica Chimica Acta, 86, 310–323.  https://doi.org/10.1002/hlca.200390033.CrossRefGoogle Scholar
  38. 38.
    Du, X., Li, Y., Xia, Y. L., Ai, S. M., Liang, J., Sang, P., & Liu, S. Q. (2016). Insights into protein–ligand interactions: mechanisms, models, and methods. International Journal of Molecular Sciences, 17(2), 1–34.  https://doi.org/10.3390/ijms17020144.CrossRefGoogle Scholar
  39. 39.
    Dellafiora, L., Galaverna, G., Reverberi, M., & Dall’Asta, C. (2017). Degradation of aflatoxins by means of laccases from Trametes versicolor: an in silico insight. Toxins, 9(1), 17.  https://doi.org/10.3390/toxins9010017.CrossRefPubMedCentralGoogle Scholar
  40. 40.
    Schrödinger, L. L. C. (2018). The PyMOL molecular graphics system. New York, USA.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • João Carlos Silva Conceição
    • 1
  • Herbert Júnior Dias
    • 2
  • Clarissa Maria Souza Peralva
    • 3
  • Antônio Eduardo Miller Crotti
    • 2
  • Samuel Silva da Rocha Pita
    • 3
  • Eliane de Oliveira Silva
    • 1
    Email author
  1. 1.Departamento de Química Orgânica, Instituto de QuímicaUniversidade Federal da BahiaSalvadorBrazil
  2. 2.Departamento de Química, Faculdade de Filosofia, Ciências e Letras de Ribeirão PretoUniversidade de São PauloRibeirão PretoBrazil
  3. 3.Laboratório de Bioinformática e Modelagem Molecular (LaBiMM), Departamento do Medicamento, Faculdade de FarmáciaUniversidade Federal da BahiaSalvadorBrazil

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