Functional annotation and comparative modeling of ligninolytic enzymes from Trametes villosa (SW.) Kreisel for biotechnological applications

References

• Ayuso‐Fernández, I., De Lacey, A., Cañada, F. J., Ruiz-Dueñas, F. J., & Martinez, A. T. (2019). Increase of redox potential during the evolution of enzymes degrading recalcitrant lignin. Chemistry (Weinheim an Der Bergstrasse, Germany), 25(11), 2708–2712. https://doi.org/10.1002/chem.201805679
   PubMed Web of Science ®Google Scholar
• Benkert, P., Biasini, M., & Schwede, T. (2011). Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics (Oxford, England), 27(3), 343–350. https://doi.org/10.1093/bioinformatics/btq662.
   PubMed Web of Science ®Google Scholar
• Benkert, P., Künzli, M., & Schwede, T. (2009). QMEAN server for protein model quality estimation. Nucleic Acids Research, 37(suppl_2), W510–514. https://doi.org/10.1093/nar/gkp322
   PubMed Web of Science ®Google Scholar
• Berman, H. M., Westbrook, Feng, J., Gilliland, Z., Bhat, G., Weissig, T. N., Shindyalov, H., & Bourne, I. N., P. E. (2000). The protein data bank. In International tables for crystallography.
   Google Scholar
• Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Cassarino, T. G., Bertoni, M., Bordoli, L., & Schwede, T. (2014). SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research, 42(W1), W252–258. https://doi.org/10.1093/nar/gku340
   PubMed Web of Science ®Google Scholar
• Blodig, W., Smith, A. T., Doyle, W. A., & Piontek, K. (2001). Crystal structures of pristine and oxidatively processed lignin peroxidase expressed in Escherichia coli and of the W171F variant that eliminates the redox active tryptophan 171. Implications for the reaction mechanism1. Journal of Molecular Biology, 305(4), 851–861. https://doi.org/10.1006/jmbi.2000.4346.
   PubMed Web of Science ®Google Scholar
• Bukh, C., Lund, M., & Bjerrum, M. J. (2006). Kinetic studies on the reaction between Trametes villosa laccase and dioxygen. Journal of Inorganic Biochemistry, 100(9), 1547–1557. https://doi.org/10.1016/j.jinorgbio.2006.05.007.
   PubMed Web of Science ®Google Scholar
• Carneiro, R. T. O., Lopes, M. A., Silva, M. L. C., Santos, V. S., de Souza, V. B., de Sousa, A., Pirovani, O., C. P., Koblitz, M. G. B., Benevides, R. G., & Góes-Neto, A. (2017). Trametes villosa lignin peroxidase (TvLiP): Genetic and molecular characterization. Journal of Microbiology and Biotechnology, 27(1), 179–188. https://doi.org/10.4014/jmb.1606.06055
   PubMed Web of Science ®Google Scholar
• Choinowski, T., Blodig, W., Winterhalter, K., & Piontek, H. K. (1999). The crystal structure of lignin peroxidase at 1.70 A resolution reveals a hydroxy group on the cbeta of tryptophan 171: a novel radical site formed during the redox cycle. Journal of Molecular Biology, 286(3), 809–827. https://doi.org/10.1006/jmbi.1998.2507.
   PubMed Web of Science ®Google Scholar
• Coconi-Linares, N., Ortiz-Vázquez, E., Fernández, F., Loske, A. M., & Gómez-Lim, M. A. (2015). Recombinant expression of four oxidoreductases in Phanerochaete chrysosporium improves degradation of phenolic and non-phenolic substrates. Journal of Biotechnology, 209, 76–84. https://doi.org/10.1016/j.jbiotec.2015.06.401.
   PubMed Web of Science ®Google Scholar
• Cohen, R., Persky, L., Hazan-Eitan, Z., Yarden, O., & Hadar, Y. (2002). Mn 2+ alters peroxidase profiles and lignin degradation by the white-rot fungus Pleurotus ostreatus under different nutritional and growth conditions. Applied Biochemistry and Biotechnology, 102–103(1–6), 415–429. https://doi.org/10.1385/ABAB:102-103:1-6:415
   PubMedGoogle Scholar
• Conesa, A., Punt, P. L., & van den Hondel, C. A. M. J. J. (2002). Fungal peroxidases: Molecular aspects and applications. Journal of Biotechnology, 93(2), 143–158. https://doi.org/10.1016/S0168-1656(01)00394-7
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Dashtban, M., Schraft, H., Syed, T. A., & Qin, W. (2010). Fungal biodegradation and enzymatic modification of lignin. International Journal of Biochemistry and Molecular Biology, 1(1), 36–50.
   PubMedGoogle Scholar
• Daura, X., van Gunsteren, W. F., & Mark, A. E. (1999). Folding–unfolding thermodynamics of a β‐heptapeptide from equilibrium simulations. Proteins: Structure, Function, and Genetics, 34(3), 269–280. https://doi.org/10.1002/(SICI)1097-0134(19990215)34:3<269::AID-PROT1>3.0.CO;2-3
   PubMed Web of Science ®Google Scholar
• Di Donato, P., Fiorentino, G., Anzelmo, G., Tommonaro, G., Nicolaus, B., & Poli, A. (2011). Re-use of vegetable wastes as cheap substrates for extremophile biomass production. Waste and Biomass Valorization, 2(2), 103–111. https://doi.org/10.1007/s12649-011-9062-x
   Web of Science ®Google Scholar
• Doyle, W. A., & Smith, A. T. (1996). Expression of lignin peroxidase H8 in Escherichia coli: Folding and activation of the recombinant enzyme with Ca2+ and haem. Biochemical Journal, 315(1), 15–19. https://doi.org/10.1042/bj3150015
   PubMedGoogle Scholar
• Eibes, G., Debernardi, G., Feijoo, G., Moreira, M. T., & Lema, J. M. (2011). Oxidation of pharmaceutically active compounds by a ligninolytic fungal peroxidase. Biodegradation, 22(3), 539–550. https://doi.org/10.1007/s10532-010-9426-0.
   PubMed Web of Science ®Google Scholar
• Ferreira, D. S. S., Kato, R. B., Miranda, F. M., da Costa Pinheiro, K., Fonseca, P. L. C., Tomé, L. M. R., Vaz, A. B. M., Badotti, F., Ramos, R. T. J., Brenig, B., Azevedo, V. A. d C., Benevides, R. G., & Góes-Neto, A. (2018). Draft genome sequence of Trametes villosa (Sw.) Kreisel CCMB561, a tropical white-rot Basidiomycota from the semiarid region of Brazil. Data in Brief, 18, 1581–1587. https://doi.org/10.1016/j.dib.2018.04.074.
   PubMed Web of Science ®Google Scholar
• Gomes, E., Aguiar, A. P., Carvalho, C. C., Maricy, Bonfá, M. R. B., da Silva, R., & Boscolo, M. (2009). Ligninases production by basidiomycetes strains on lignocellulosic agricultural residues and their application in the decolorization of synthetic dyes. Brazilian Journal of Microbiology : [Publication of the Brazilian Society for Microbiology], 40(1), 31–39. https://doi.org/10.1590/S1517-83822009000100005
   PubMed Web of Science ®Google Scholar
• Grigoriev, I. V., Nikitin, R., Haridas, S., Kuo, A., Ohm, R., Otillar, R., Riley, R., Salamov, A., Zhao, X., Korzeniewski, F., Smirnova, T., Nordberg, H., Dubchak, I., & Shabalov, I. (2014). MycoCosm portal: Gearing up for 1000 fungal genomes. Nucleic Acids Research, 42(D1), D699–704. https://doi.org/10.1093/nar/gkt1183
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
   Web of Science ®Google Scholar
• Holtje, H. D., Folkers, G., Mannhold, R., Kubinyi, H., & Timmerman, H. H. (1997). Molecular modeling: basic principles and applications. John Wiley & Sons.
   Google Scholar
• Huang, S. T., Tzean, S. S., Tsai, B. Y., & Hsieh, H. J. (2009). Cloning and heterologous expression of a novel ligninolytic peroxidase gene from poroid brown-rot fungus Antrodia cinnamomea. Microbiology (Reading, England), 155(Pt 2), 424–433. https://doi.org/10.1099/mic.0.022459-0.
   PubMedGoogle Scholar
• Janusz, G., Kucharzyk, K. H., Pawlik, A., Staszczak, M., & Paszczynski, A. J. (2013). Fungal laccase, manganese peroxidase and lignin peroxidase: Gene expression and regulation. Enzyme and Microbial Technology, 52(1), 1–12. https://doi.org/10.1016/j.enzmictec.2012.10.003
   PubMed Web of Science ®Google Scholar
• Johansson, T., & Nyman, P. O. (1996). A cluster of genes encoding major isozymes of lignin peroxidase and manganese peroxidase from the white-rot fungus Trametes versicolor. Gene, 170(1), 31–38. https://doi.org/10.1016/0378-1119(95)00846-2
   PubMed Web of Science ®Google Scholar
• Justo, A., & Hibbett, D. S. (2011). Phylogenetic classification of Trametes (Basidiomycota, Polyporales) based on a five-marker dataset. TAXON, 60(6), 1567–1583. https://doi.org/10.1002/tax.606003
   Web of Science ®Google Scholar
• Kale, S. K., & Deshmukh, A. G. (2016). 3D structure prediction of lignolytic enzymes lignin peroxidase and manganese peroxidase based on homology modelling. Journal of BioScience & Biotechnology, 5, 1–11.
   Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Malde, A. K., Zuo, L., Breeze, M., Stroet, M., Poger, D., Nair, P. C., Oostenbrink, C., & Mark, A. E. (2011). An automated force field topology builder (ATB) and repository: Version 1.0. Journal of Chemical Theory and Computation, 7(12), 4026–4037. https://doi.org/10.1021/ct200196m
   PubMed Web of Science ®Google Scholar
• Martinez, A. T. (2002). Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzyme and Microbial Technology, 30, 425–444. https://doi.org/10.1016/s0141-0229(01)00521-x.
   Web of Science ®Google Scholar
• Melo, F., Devos, D., Depiereux, E., Feytmans, E. (1997). ANOLEA: a www server to assess protein structures. In Ismb (Vol. 5, pp. 187–190).
   Google Scholar
• Neves, M. A., Baseia, I. G., Drechsler-Santos, E. R., & Góes-Neto, A. (2013). Guide to the common fungi of semiarid region of Brazil. TECC.
   Google Scholar
• Overbeek, R., Disz, T., & Stevens, R. (2004). The SEED: A peer-to-peer environment for genome annotation. Communications of the ACM, 47(11), 46–51. https://doi.org/10.1145/1029496.1029525
   Web of Science ®Google Scholar
• Pavlov, A. R., Tyazhelova, T. V., Moiseenko, K. V., Vasina, D. V., Mosunova, O. V., Fedorova, T. V., Maloshenok, L. G., Landesman, E. O., Bruskin, S. A., Psurtseva, N. V., Slesarev, A. I., Kozyavkin, S. A., & Koroleva, O. V. (2015). Draft genome sequence of the fungus Trametes hirsuta 072. Genome Announcements, 3(6). https://doi.org/10.1128/genomeA.01287-15
   Google Scholar
• Petersen, T. N., Brunak, S., von Heijne, G., & Nielsen, H. (2011). SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nature Methods, 8(10), 785–786. https://doi.org/10.1038/nmeth.1701.
   PubMed Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera-a visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084.
   PubMed Web of Science ®Google Scholar
• Pierleoni, A., Martelli, P. L., Fariselli, P., & Casadio, R. (2006). BaCelLo: A balanced subcellular localization predictor. Bioinformatics (Oxford, England), 22(14), e408–416. https://doi.org/10.1093/bioinformatics/btl222
   PubMed Web of Science ®Google Scholar
• Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., & Lindahl, E. (2013). GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics (Oxford, England), 29(7), 845–854. https://doi.org/10.1093/bioinformatics/btt055.
   PubMed Web of Science ®Google Scholar
• Recabarren, R., Fuenzalida-Valdivia, I., & Alzate-Morales, J. (2016). Studying the binding mechanisms of veratryl alcohol to P. chrysosporium lignin peroxidase: Insights from theoretical approaches. Theoretical Chemistry Accounts, 135(3), 1–12. https://doi.org/10.1007/s00214-016-1828-6
   Web of Science ®Google Scholar
• Riley, R., Salamov, A. A., Brown, D. W., Nagy, L. G., Floudas, D., Held, B. W., Levasseur, A., Lombard, V., Morin, E., Otillar, R., Lindquist, E. A., Sun, H., LaButti, K. M., Schmutz, J., Jabbour, D., Luo, H., Baker, S. E., Pisabarro, A. G., Walton, J. D., … Grigoriev, I. V. (2014). Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proceedings of the National Academy of Sciences of the United States of America, 111(27), 9923–9928. https://doi.org/10.1073/pnas.1400592111.
   PubMed Web of Science ®Google Scholar
• Rostkowski, M., Olsson, M. H., Søndergaard, C. R., & Jensen, J. H. (2011). Graphical analysis of pH-dependent properties of proteins predicted using PROPKA. BMC Structural Biology, 11, 6. https://doi.org/10.1186/1472-6807-11-6.
   PubMed Web of Science ®Google Scholar
• Ruiz-Dueñas, F. J., Fernández, E., Martínez, M. J., & Martínez, A. T. (2011). Pleurotus ostreatus heme peroxidases: An in silico analysis from the genome sequence to the enzyme molecular structure. Comptes rendus biologies, 334(11), 795–805. https://doi.org/10.1016/j.crvi.2011.06.004.
   PubMed Web of Science ®Google Scholar
• Ruiz-Duenas, F. J., Morales, M., Garcia, E., Miki, Y., Martinez, M. J., & Martinez, A. T. (2009). Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. Journal of Experimental Botany, 60(2), 441–452. https://doi.org/10.1093/jxb/ern261.
   PubMed Web of Science ®Google Scholar
• Schrödinger, L. L. C. (2016). PyMol: the PyMOL molecular graphics system, version 2.0. Schrödinger LLC.
   Google Scholar
• Shukla, A., Gundampati, R. K., Rajasekhar, C., & Jagannadham, M. V. (2016). Homology modeling and molecular docking of heme peroxidase from Euphorbia tirucalli: Substrate specificity and thiol inhibitor interactions. Journal of Molecular Liquids, 220, 383–394. https://doi.org/10.1016/j.molliq.2016.04.102
   Web of Science ®Google Scholar
• Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., & Higgins, D. G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7, 539. https://doi.org/10.1038/msb.2011.75
   PubMed Web of Science ®Google Scholar
• Silva, M. L. C., Souza, V. B. D., Santos, V. D. S., Kamida, H. M., Vasconcellos-Neto, J. R. T. D., Góes-Neto, A., & Bello Koblitz, M. G. (2014). Production of manganese peroxidase by Trametes villosa on unexpensive substrate and its application in the removal of lignin from agricultural wastes. Advances in Bioscience and Biotechnology, 5(14), 1067–2014. https://doi.org/10.4236/abb.2014.514122
   Google Scholar
• Stanke, M., & Morgenstern, B. (2005). AUGUSTUS: A web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Research, 33(suppl_2), W465–467. https://doi.org/10.1093/nar/gki458
   PubMedGoogle Scholar
• Taurisano, V., Anzelmo, G., Poli, A., Nicolaus, B., & Di Donato, P. (2014). Re-use of agro-industrial waste: Recovery of valuable compounds by eco-friendly techniques. International Journal of Performability Engineering, 10, 419–425.
   Google Scholar
• Verlet, L. (1967). Computer “Experiments” on Classical Fluids. I. Thermodynamical Properties of Lennard-Jones Molecules. Physical Review, 159(1), 98–103. https://doi.org/10.1103/PhysRev.159.98
   Web of Science ®Google Scholar
• Verli, H. (2014). Bioinformática: da biologia à flexibilidade molecular.,
   Google Scholar
• Wang, W., & Wen, X. (2009). Expression of lignin peroxidase H2 from Phanerochaete chrysosporium by multi-copy recombinant Pichia strain. Journal of Environmental Sciences, 21(2), 218–222. https://doi.org/10.1016/S1001-0742(08)62254-8
   Google Scholar
• Webb, B., & Sali, A. (2014). Comparative Protein Structure Modeling Using MODELLER. Curr Protoc Bioinformatics, 47, 5.6.1–6.32. https://doi.org/10.1002/0471250953.bi0506s47.
   PubMedGoogle Scholar
• Wheeler, D. L., Chappey, C., Lash, A. E., Leipe, D. D., Madden, T. L., Schuler, G. D., Tatusova, T. A., & Rapp, B. A. (2000). Database resources of the National Center for Biotechnology Information. Nucleic Acids Research, 28(1), 10–14. https://doi.org/10.1093/nar/28.1.10.
   PubMed Web of Science ®Google Scholar
• Wong, D. W. S. (2009). Structure and action mechanism of ligninolytic enzymes. Applied Biochemistry and Biotechnology, 157(2), 174–209. https://doi.org/10.1007/s12010-008-8279-z.
   PubMed Web of Science ®Google Scholar
• Yaver, D. S., Xu, F., Golightly, E. J., Brown, K. M., Brown, S. H., Rey, M. W., Schneider, P., Halkier, T., Mondorf, K., & Dalboge, H. (1996). Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Applied and Environmental Microbiology, 62(3), 834–841. https://doi.org/10.1128/AEM.62.3.834-841.1996
   PubMed Web of Science ®Google Scholar
• Zámocký, M., Hofbauer, S., Schaffner, I., Gasselhuber, B., Nicolussi, A., Soudi, M., Pirker, K. F., Furtmüller, P. G., & Obinger, C. (2015). Independent evolution of four heme peroxidase superfamilies. Archives of Biochemistry and Biophysics, 574, 108–119. https://doi.org/10.1016/j.abb.2014.12.025
   PubMed Web of Science ®Google Scholar
• Zhang, L., & Skolnick, J. (1998). What should the Z-score of native protein structures be? Protein Science : a Publication of the Protein Society, 7(5), 1201–1207. https://doi.org/10.1002/pro.5560070515
   PubMed Web of Science ®Google Scholar
• Zimmermann, L., Stephens, A., Nam, S.-Z., Rau, D., Kübler, J., Lozajic, M., Gabler, F., Söding, J., Lupas, A. N., & Alva, V. (2018). A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. Journal of Molecular Biology, 430(15), 2237–2243. https://doi.org/10.1016/j.jmb.2017.12.007.
   PubMed Web of Science ®Google Scholar