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3 Biotech

, 9:160 | Cite as

Molecular characterization of laccase genes from the basidiomycete Trametes hirsuta Bm-2 and analysis of the 5′ untranslated region (5′UTR)

  • Alejandrina Pereira-Patrón
  • Sara Solis-Pereira
  • Gabriel Lizama-Uc
  • Jorge H. Ramírez-Prado
  • Daisy Pérez-Brito
  • Raul Tapia-TussellEmail author
Original Article

Abstract

The aim of this study was to identify and characterize laccase genes produced by Trametes hirsuta Bm-2 in a liquid medium, both with and without induction. The amplification of 5′and 3′regions of laccase sequences was obtained by the RACE-PCR method, and these were assembled to obtain a cDNA of total length. Two new laccase genes were isolated from basal medium (lac-B) and lignocellulosic grapefruit substrate (lac-T), both encoding open reading frames of 2566 bp. Both laccase-predicted proteins consisted of 521 amino acids, four copper-binding regions, a signal peptide, and five potential glycosilation sites (Asn-Xaa-Ser/Tre). Moreover, the deduced amino acid sequences share about 76–85% identity with other laccases of WRF. Sequence comparison showed 47 synonymous point mutations between lac-B and lac-T. In addition, 5′ untranslated regions (UTR) of laccase genes lac-B and lac-T showed differences in length and number of regulatory elements that may affect transcriptional or translational expression of these genes.

Keywords

Trametes hirsuta Laccase genes RACE-PCR Untranslated regions 

Notes

Acknowledgement

The authors wish to express their gratitude to National Science and Technology Council, Mexico (CONACYT) for providing the financial support for this research (Project No. 248295).

Author contributions

All the authors contributed to this work. Tapia-Tussell and Solis-Pereira conceived, designed and wrote the paper; Pereira-Patron performed the experiments and analyzed the data; Lizama-Uc, Perez-Brito and Ramirez-Prado participated in the data analysis of untranslated region and writing of the paper. All authors reviewed and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest regarding publication of this paper.

References

  1. Altschul SF, Madden TL, Schäffer AA et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  2. Asgher M, Yasmeen Q, Iqbal HMN (2014) Development of novel enzymatic bioremediation process for textile industry effluents through response surface methodology. Ecol Eng 63:1–11CrossRefGoogle Scholar
  3. Baldrian P (2006) Fungal laccases–occurrence and properties. FEMS Microbiol Rev 30:215–242CrossRefGoogle Scholar
  4. Barrett LW, Fletcher S, Wilton SD (2013) Untranslated gene regions and other non-coding elements. In: Untranslated Gene Regions and Other Non-coding Elements. Springer, pp 1–56Google Scholar
  5. Bradnam KR, Korf I (2008) Longer first introns are a general property of eukaryotic gene structure. PLoS ONE 3:e3093CrossRefGoogle Scholar
  6. Brijwani K, Rigdon A, Vadlani PV (2010) Fungal laccases: production, function, and applications in food processing. Enzyme Res 2010:149748CrossRefGoogle Scholar
  7. Bruno VM, Wang Z, Marjani SL et al (2010) Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res. 20(10):1451–1458CrossRefGoogle Scholar
  8. Bulter T, Alcalde M, Sieber V et al (2003) Functional expression of a fungal laccase in Saccharomyces cerevisiae by directed evolution. Appl Environ Microbiol 69:987–995CrossRefGoogle Scholar
  9. Dmitriev SE, Andreev DE, Ad’ianova ZV et al (2009) Efficient cap-dependent in vitro and in vivo translation of mammalian mRNAs with long and highly structured 5′-untranslated regions. Mol Biol (Mosk) 43:119–125CrossRefGoogle Scholar
  10. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefGoogle Scholar
  11. Feng BZ, Li PQ, Fu L, Yu XM (2015) Exploring laccase genes from plant pathogen genomes: a bioinformatic approach. Genet Mol Res 14:14019–14036CrossRefGoogle Scholar
  12. Ganapathi M, Srivastava P, Das Sutar SK et al (2005) Comparative analysis of chromatin landscape in regulatory regions of human housekeeping and tissue specific genes. BMC Bioinform 6:126CrossRefGoogle Scholar
  13. Givaudan A, Effosse A, Faure D et al (1993) Polyphenol oxidase in Azospirillum lipoferum isolated from rice rhizosphere: evidence for laccase activity in non-motile strains of Azospirillum lipoferum. FEMS Microbiol Lett 108:205–210CrossRefGoogle Scholar
  14. Gupta R, Brunak S (2001) Prediction of glycosylation across the human proteome and the correlation to protein function. In: Biocomputing 2002. World Scientific, pp 310–322Google Scholar
  15. Jin W, Li J, Feng H et al (2018) Importance of a laccase gene (Lcc1) in the development of Ganoderma tsugae. Int J Mol Sci 19:471CrossRefGoogle Scholar
  16. Kalyani D, Tiwari MK, Li J et al (2015) A highly efficient recombinant laccase from the yeast Yarrowia lipolytica and its application in the hydrolysis of biomass. PLoS ONE 10:e0120156CrossRefGoogle Scholar
  17. Kandasamy S, Muniraj IK, Purushothaman N et al (2016) High level secretion of laccase (LccH) from a newly isolated white-rot basidiomycete, Hexagonia hirta MSF2. Front Microbiol 7:707CrossRefGoogle Scholar
  18. Kikin O, D’Antonio L, Bagga PS (2006) QGRS Mapper: a web-based server for predicting G-quadruplexes in nucleotide sequences. Nucleic Acids Res 34:W676–W682CrossRefGoogle Scholar
  19. Kim J-K, Lim S-H, Kang H-W (2013) Cloning and characterization of a novel laccase gene, fvlac7, based on the genomic sequence of Flammulina velutipes. Mycobiology 41:37–41CrossRefGoogle Scholar
  20. Kim H-I, Kwon O-C, Kong W-S et al (2014) Genome-wide identification and characterization of novel laccase genes in the white-rot fungus Flammulina velutipes. Mycobiology 42:322–330CrossRefGoogle Scholar
  21. Kirk TK, Croan S, Tien M et al (1986) Production of multiple ligninases by Phanerochaete chrysosporium: effect of selected growth conditions and use of a mutant strain. Enzyme Microb Technol 8:27–32CrossRefGoogle Scholar
  22. Kochetov AV, Ischenko IV, Vorobiev DG et al (1998) Eukaryotic mRNAs encoding abundant and scarce proteins are statistically dissimilar in many structural features. FEBS Lett 440:351–355CrossRefGoogle Scholar
  23. Kolekar P, Pataskar A, Kulkarni-Kale U et al (2016) IRESPred: web server for prediction of cellular and viral internal ribosome entry site (IRES). Sci Rep 6:27436CrossRefGoogle Scholar
  24. Kozak M (1989) The scanning model for translation: an update. J Cell Biol 108:229–241CrossRefGoogle Scholar
  25. Kumar SVS, Phale PS, Durani S, Wangikar PP (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83:386–394CrossRefGoogle Scholar
  26. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  27. Kunamneni A, Plou FJ, Ballesteros A, Alcalde M (2008) Laccases and their applications: a patent review. Recent Pat Biotechnol 2:10–24CrossRefGoogle Scholar
  28. Lin Z, Li W-H (2011) Evolution of 5′ untranslated region length and gene expression reprogramming in yeasts. Mol Biol Evol 29:81–89CrossRefGoogle Scholar
  29. Mignone F, Gissi C, Liuni S, Pesole G (2002) Untranslated regions of mRNAs. Genome Biol 3:0004CrossRefGoogle Scholar
  30. Morozova OV, Shumakovich GP, Shleev SV, Yaropolov YI (2007) Laccase-mediator systems and their applications: a review. Appl Biochem Microbiol 43:523–535CrossRefGoogle Scholar
  31. Nagalakshmi U, Wang Z, Waern K et al (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science. 320:1344–1349CrossRefGoogle Scholar
  32. Nielsen H (2017) Predicting secretory proteins with SignalP. Protein Funct Predict Methods Protoc. 1:59–73CrossRefGoogle Scholar
  33. Palanisamy S, Ramaraj SK, Chen S-M et al (2017) A novel laccase biosensor based on laccase immobilized graphene-cellulose microfiber composite modified screen-printed carbon electrode for sensitive determination of catechol. Sci Rep 7:41214CrossRefGoogle Scholar
  34. Park Y-J, Yoon D-E, Kim H-I et al (2014) Overproduction of laccase by the white-rot fungus Pleurotus ostreatus using apple pomace as inducer. Mycobiology 42:193–197CrossRefGoogle Scholar
  35. Pickering BM, Willis AE (2005) The implications of structured 5′ untranslated regions on translation and disease. In: Seminars in cell & developmental biology. Elsevier, New York, pp 39–47Google Scholar
  36. Tapia-Tussell R, Pérez-Brito D, Rojas-Herrera R et al (2011) New laccase-producing fungi isolates with biotechnological potential in dye decolorization. Afr J Biotechnol 10:10134–10142CrossRefGoogle Scholar
  37. Teerapatsakul C, Abe N, Bucke C et al (2007) Novel laccases of Ganoderma sp. KU-Alk4, regulated by different glucose concentration in alkaline media. World J Microbiol Biotechnol 23:1559–1567CrossRefGoogle Scholar
  38. Téllez-Jurado A, Arana-Cuenca A, Becerra AEG et al (2006) Expression of a heterologous laccase by Aspergillus niger cultured by solid-state and submerged fermentations. Enzyme Microb Technol 38:665–669CrossRefGoogle Scholar
  39. Terrón MC, González T, Carbajo JM et al (2004) Structural close-related aromatic compounds have different effects on laccase activity and on lcc gene expression in the ligninolytic fungus Trametes Trametes sp. I-62. Fungal Genet Biol 41:954–962CrossRefGoogle Scholar
  40. Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26CrossRefGoogle Scholar
  41. Uthandi S, Saad B, Humbard MA, Maupin-Furlow JA (2010) LccA, an archaeal laccase secreted as a highly stable glycoprotein into the extracellular medium by Haloferax volcanii. Appl Environ Microbiol 76:733–743CrossRefGoogle Scholar
  42. Vasina DV, Mustafaev ON, Moiseenko KV et al (2015) The Trametes hirsuta 072 laccase multigene family: genes identification and transcriptional analysis under copper ions induction. Biochimie 116:154–164CrossRefGoogle Scholar
  43. Viswanath B, Rajesh B, Janardhan A et al (2014) Fungal laccases and their applications in bioremediation. Enzyme Res 2014:163242CrossRefGoogle Scholar
  44. Vite-Vallejo O, Palomares LA, Dantán-González E et al (2009) The role of N-glycosylation on the enzymatic activity of a Pycnoporus sanguineus laccase. Enzyme Microb Technol 45:233–239CrossRefGoogle Scholar
  45. Wang W, Liu F, Jiang Y et al (2015) The multigene family of fungal laccases and their expression in the white rot basidiomycete s. Flammulina velutipes. Gene 563:142–149CrossRefGoogle Scholar
  46. Yang J, Xu X, Ng TB et al (2016) Laccase gene family in Cerrena sp. HYB07: sequences, heterologous expression and transcriptional analysis. Molecules 21:1017CrossRefGoogle Scholar
  47. Zapata-Castillo P, Villalonga-Santana M, Tamayo-Cortés J et al (2012) Purification and characterization of laccase from Trametes hirsuta Bm-2 and its contribution to dye and effluent decolorization. Afr J Biotechnol 11:3603–3611Google Scholar
  48. Zapata-Castillo P, Villalonga-Santana L, Islas-Flores I et al (2015) Synergistic action of laccases from Trametes hirsuta Bm2 improves decolourization of indigo carmine. Lett Appl Microbiol 61:252–258CrossRefGoogle Scholar
  49. Zhou YP, Chen QH, Xiao YN et al (2014) Gene cloning and characterization of a novel laccase from the tropical white-rot fungus Ganoderma weberianum TZC-1. Appl Biochem Microbiol 50:500–507CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  1. 1.Depto. de Ingeniería Química y Bioquímica, Tecnológico Nacional de México, Instituto Tecnológico de MéridaMéridaMexico
  2. 2.Unidad de Biotecnología, Centro de Investigación Científica de YucatánMéridaMexico
  3. 3.Laboratorio GeMBioCentro de Investigación Científica de YucatánMéridaMexico
  4. 4.Unidad de Energía Renovable, Centro de Investigación Científica de YucatánMéridaMexico

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