Advertisement

3 Biotech

, 9:297 | Cite as

Determination of the effect of RBBR on laccase activity and gene expression level of fungi in lichen structure

  • Elif Değerli
  • Sevcan Yangın
  • Demet Cansaran-DumanEmail author
Original Article
  • 35 Downloads

Abstract

This study provides information about the differential transcription regulation of laccase genes in response to RBBR dye. To this purpose, we determined the laccase gene expression, laccase activity, and protein profile of lichen-forming fungi supported to RBBR dye. For those obtained from optimal laccase genes expression profiles, we modified different RNA extraction protocols to obtain high quality and quantity RNA to be used in downstream applications in lichen-forming fungus. We also determined the expression of ten laccase genes in response to RBBR dye by qRT-PCR and validated protein profile. As a result of our study, a high laccase activity of 522 U mL−1 was obtained after submerged fermentation for 17 days. The maximal laccase activity to RBBR dye was obtained at 408 h. The expression profiles of laccase gene expression on ten laccase genes showed up- or down-regulation in course of eight fermentation times. The most up-regulated gene during the process was lac8. However, poxa1b gene expression was lowest in lichen-forming fungi biomass supplemented with RBBR dye. This study has revealed the influence of RBBR dye on laccase activity levels and the determination of gene expression levels in lichen-forming fungi.

Keywords

Laccase activity RBBR RNA extraction Laccase gene expression Lichen-forming fungi 

Notes

Acknowledgements

We would like to thank the Ankara University Project Offices, Project No. 13H4143001, for the partial financial support.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest, and that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Research involving human participants and/or animals

This article does not involve any studies conducted on human participants or animals, carried out by any of the authors.

References

  1. Abadulla E, Tzanov T, Costa S, Robra KH, Cavaco-Paulo A, Gübitz GM (2000) Decolorization and detoxification of textile dyes with a laccase from Trametes hirsuta. Appl Environ Microbiol 66:3357–3362CrossRefGoogle Scholar
  2. Anastasi A, Spina F, Romagnolo A, Tigini V, Prigioni V, Varese GC (2012) Integrated fungal biomass and activated sludge treatment for wastewater bioremediation. Bioresour Technol 123:106–111CrossRefGoogle Scholar
  3. Backorova M, Jendzelovsky R, Kello M, Backor M, Mikes J, Fedorocko P (2012) Lichen secondary metabolites are responsible for induction of apoptosis in HT-29 and A2780 human cancer cell lines. Toxicol In Vitro 26(3):462–468CrossRefGoogle Scholar
  4. Baldrian P (2006) Fungallaccases-occurrence and properties. FEMS Microbiol Rev 30:215–242CrossRefGoogle Scholar
  5. Bankole (2017) Environmental chemistry, pollution, waste management research article. Cogent Environ Sci 3:1278646CrossRefGoogle Scholar
  6. Bertrand B, Martínez-Morales F, Tinoco-Valencia R, Rojas S, Acosta-Urdapilleta L, Trejo-Hernández MR (2015) Biochemical and molecular characterization of laccase isoforms produced by the white-rot fungus Trametes versicolor under submerged culture conditions. J Mol Catal Enzym 122:339–347CrossRefGoogle Scholar
  7. Birhanlı E, Yeşilada Ö (2006) Increased production of laccase by pellets of Funalia trogii ATCC 200800 and Trametes versicolor ATCC 200801 in repeated-batch mode. Enzyme Microb Technol 39:1286–1293CrossRefGoogle Scholar
  8. Birhanlı E, Yeşilada Ö (2013) The utilization of lingo cellulosic wastes for laccase production under semisolid-state and submerged fermentation conditions. Turk J Biol 37:450–456CrossRefGoogle Scholar
  9. Cansaran-Duman D, Altunkaynak E, Aras S (2014) Heavy metal accumulation and genotoxicity indicator capacity of the lichen species, Ramalina pollinaria collected from around an iron-steel factory in Karabük, Turkey. Turk J Bot 38:477–490CrossRefGoogle Scholar
  10. Chakroun H, Mechichi T, Martinez MJ, Dhouib A, Sayadi S (2010) Purification and characterization of a novel laccase from the ascomycete Trichoderma atroviride: application on bioremediation of phenolic compounds. Process Biochem 45:507–513CrossRefGoogle Scholar
  11. Claus H (2003) Laccases and their occurrence in prokaryotes. Archiv Microbiol 179(3):145–150CrossRefGoogle Scholar
  12. Couto RS, Toca Herrera JL (2006) Industrial and biotechnological applications of laccases: a review. Biotechnol Adv 24:500–513CrossRefGoogle Scholar
  13. Daneshwar N, Ayazloo M, Khataee AR, Pourhassan M (2007) Biological decolorization of dye solution containing malachite green by microalgae Cosmarium sp. Bioresour Technol 98:1176–1182CrossRefGoogle Scholar
  14. Demiralp B, Büyük İ, Aras S, Cansaran-Duman D (2015) Industrial and biotechnological applications of laccase enzyme. Türk Hij Den Biol Derg 72(4):351–368CrossRefGoogle Scholar
  15. Derici MK, Cansaran-Duman D, Taylan-Özkan A (2018) Usnic acid causes apoptotic-like death in Leishmania major, L. infantum and L. tropica. 3 Biotech 8:384CrossRefGoogle Scholar
  16. Díaz R, Saparrat MCN, Jurado M, García-Romera I, Ocampo JA, Martínez MJ (2010) Biochemical and molecular characterization of Coriolopsis rigida laccases involved in transformation of the solid waste from olive oil production. Appl Microbiol Biotechnol 88:133–142CrossRefGoogle Scholar
  17. Dinçsoy AB, Cansaran-Duman D (2017) Changes in apoptosis related gene expression profiles in cancer cell line exposed to usnic acid lichen secondary metabolite. Turk J Biol 41:484–493CrossRefGoogle Scholar
  18. Durán N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99CrossRefGoogle Scholar
  19. Duran N, Rosa MA, D'Annibale A, Gianfreda L (2002) Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzym Icrob Technol 31:907–931CrossRefGoogle Scholar
  20. Galhaup CGS, Galhaup C, Goller S, Peterbauer CK, Strauss J, Haltrich D (2002) Characterization of the major laccase isoenzyme from Trametes pubescens and regulation of its synthesis by metal ions. Microbiology 148:2159–2169CrossRefGoogle Scholar
  21. Garrido-Bazan V, Tellez-Tellez M, Herrera-Estrella A, Diaz-Godinez G, Nava-Galicia S, Villalobos-Lopez MA, Arroyo-Becerra A, Bibbins-Martinez M (2016) Effect of textile dyes on activity and differential regulation of laccase genes from Pleurotus ostreatus grown in submerged fermentation. AMB Expr 6:93CrossRefGoogle Scholar
  22. Humnabadkar RP, Saratale GD, Govindwar SP (2008) Decolorization on purple 2Rby Aspergillus ochraceus (NCIM-1146). Asian J Microbiol Biotechnol Environ Sci 10:693–697Google Scholar
  23. Husain Q (2006) Potential applications of the oxidoreductive enzymes in the decolorization and detoxification of textile and other synthetic dyes from polluted water: a review. Crit Rev Biotechnol 26:201–221CrossRefGoogle Scholar
  24. Jadhav JP, Govindwar SP (2006) Biotransformation of malachite green by Saccharomyces cerevisiae MTCC 463. Yeast 23:315–323CrossRefGoogle Scholar
  25. Janusz G, Kucharzyk KH, Pawlik A, Staszczak M, Paszczynski AJ (2013) Fungal laccase, manganese peroxidase and lignin peroxidase: gene expression and regulation. Enzyme Microb Technol 52:1–12CrossRefGoogle Scholar
  26. Jin X, Ning Y (2013) Laccase production optimization by response surface methodology with Aspergillus fumigatus AF1 in unique inexpensive medium and decolorization of different dyes with the crude enzyme or fungal pellets. J Hazard Mater 262:870–877.  https://doi.org/10.1016/j.jhazmat.2013.09.024 CrossRefPubMedGoogle Scholar
  27. Junttila S, Kean-Jin L, Stephen R (2009) Optimization and comparison of different methods for RNA isolation for cDNA library construction from the reindeer lichen Cladonia rangiferina. BMC Res Notes 2:204CrossRefGoogle Scholar
  28. Kagalkar AN, Jagtap UB, Govindwar SP, Jadhav JP, Bapat VA (2010) Studies on phytoremediation potentiality of Typhonium flagelliforme for the degradation of Brilliant Blue R. Planta 232:271–328CrossRefGoogle Scholar
  29. Kaushik P, Malik A (2009) Fungal dye decolourization: recent advances and future potential. Environ Int 35(1):127–141.  https://doi.org/10.1016/j.envint.2008.05.010 CrossRefPubMedGoogle Scholar
  30. Kılıç Z, Atakol O, Aras S, Cansaran-Duman D, Çelikkol P, Emregul E (2014) Evaluation of different isotherm models, kinetic, thermodynamic and copper biosorption efficiency of Lobaria pulmonaria (L.) Hoffm. J Air Waste Manag Assoc 64(1):115–123CrossRefGoogle Scholar
  31. Kılıç N, Nasiri F, Cansaran-Duman D (2016) Phytoremediation. Management of environmental contaminants. In: Ansari AA (ed) Fungal laccase enzyme applications in bioremediation of polluted wastewater, vol 4. Springer, Boston, pp 201–209. ISBN 978-3-319-41810-0CrossRefGoogle Scholar
  32. Kılıç N, Derici K, Büyük İ, Soydam-Aydın S, Aras S, Cansaran-Duman D (2018) Evaluation of in vitro anticancer activity of vulpinic acid and its apoptotic potential using gene expression and protein analysis. Indian J Pharm Edu Res 52(3):46–54Google Scholar
  33. Kramer KJ (2001) Oxidative conjugation of catechols with proteins in insect skeletal systems. Tetrahedron 57:385–392CrossRefGoogle Scholar
  34. Kulkarni AN, Kadamb AA, Kacholec MS, Govindwar SP (2014) Lichen Parmelia perlata: a novel system for biodegradation and detoxification of disperse dye Solvent Red 24. J Hazard Mat 276:461–468CrossRefGoogle Scholar
  35. Kumar A, Sharma KK, Kumar P, Ramchiary N (2015) Laccase isozymes from Ganoderma lucidum MDU-7: isolation, characterization, catalytic properties and differential role during oxidative stress. J Mol Catal B Enzym 113:68–75CrossRefGoogle Scholar
  36. Laufer Z, Beckett RP, Minibayeva FV, Luthje S, Bottger M (2006a) Occurrence of laccases in lichenized ascomycetes of the Peltigerineae. Mycol Res 110:846–853CrossRefGoogle Scholar
  37. Laufer Z, Beckett RP, Minibayeva FV (2006b) Co-occurrence of the multicopper oxidases tyrosinase and laccase in lichens in sub-order peltigerineae. Ann Bot 98:1035–1042CrossRefGoogle Scholar
  38. Lisov AV, Zavarzina AG, Alexey AZ, Alexey AL (2007) Laccases produced by lichens of the order Peltigerales. FEMS Microbiol Lett 275:46–52CrossRefGoogle Scholar
  39. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta DeltaC(T)) method. Methods 25(4):402–408CrossRefGoogle Scholar
  40. Mostafa ME, Gharieb MM, Abou-El-Souod GW (2009) Biodegradation of dyes by some green algae and cyanobacteria. Int Biodeterior Biodegrad 63:699–704CrossRefGoogle Scholar
  41. Muggia L, Grube M (2018) Fungal diversity in lichens: from extremo tolerance to interactions with algae. Life 8:15CrossRefGoogle Scholar
  42. Novotny C, Svobodova K, Benada O, Kofronova O, Heissenberger A, Fuchs W (2011) Potential of combined fungal and bacterial treatment for color removal in textile wastewater. Bioresour Technol 102:879–888CrossRefGoogle Scholar
  43. Pezzella C, Lettera V, Piscitelli A, Giardina P, Sannia G (2012) Transcriptional analysis of Pleurotus ostreatus laccase genes. Appl Microbiol Biotechnol 97:705–717CrossRefGoogle Scholar
  44. Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011) Induction and transcriptional regulation of laccases in fungi. Curr Genom 12:104–112.  https://doi.org/10.2174/138920211795564331 CrossRefGoogle Scholar
  45. Schumann U, Neil AS, Ming-Bo W (2013) A fast and efficient method for preparation of high-quality RNA from fungal mycelia. BMC Res Notes 6:71CrossRefGoogle Scholar
  46. Schwarzenbach RP, Escher BI, Fenner K, Hofstetter TB, Johnson CA, von-Gunten U, Wehrli B (2006) The challenge of micro-pollutants in aquatic systems. Science 313:1072–1077CrossRefGoogle Scholar
  47. Shrestha G, Thompson A, Robison R, Larry L, Clair L (2015) Letharia vulpina, a vulpinic acid containing lichen, targets cell membrane and cell division processes in methicillin resistant Staphylococcus aureus. Pharm Biol 54(3):413–418CrossRefGoogle Scholar
  48. Singh K, Arora S (2011) Removal of synthetic textile dyes from wastewaters: a critical review on present treatment technologies. Crit Rev Environ Sci Technol 41(9):807–878CrossRefGoogle Scholar
  49. Soden DM, Dobson AD (2001) Differential regulation of laccase gene expression in Pleurotus sajor-caju. Microbiol 147:1755–1763CrossRefGoogle Scholar
  50. Sokolovsky V, Kaldenhoff R, Ricci M, Russo VEA (1990) Fast and reliable mini-prep RNA extraction from Neurospora crassa. Fungal Genet Newsl 37:41–43Google Scholar
  51. Suzuki M, Ketterling MG, Mccarty DR (2005) Quantitative statistical analysis of cis-regulatory sequences in ABA/VP1- and CBF/DREB1-regulated genes of Arabidopsis. Plant Physiol 139(1):437–447CrossRefGoogle Scholar
  52. Tellez-Tellez M, Fernandez FJ, Montiel-Gonzalez AM, Sanchez C, Diaz-Godinez G (2008) Growth and laccase production by Pleurotus ostreatus in submerged and solid-state fermentation. Appl Microbiol Biotechnol 81(4):675–679CrossRefGoogle Scholar
  53. Untergasser A (2008) DNA Miniprep using CTAB. Untergasser’s Lab. Summer. http://www.untergasser.de/lab/protocols/miniprep_dna_ctab_v1. Accessed 18 Oct 2008
  54. Waghmode TR, Kurade MB, Govindwar SP (2011) Time dependent degradation of mixture of structurally different azo and non azo dyes by using Galactomyces geotrichum MTCC 1360. Int Biodeterior Biodegrad 65:479–486CrossRefGoogle Scholar
  55. Xiao YZ, Hong YZ, Li JF, Hang J, Tong PG, Fang W (2006) Cloning of novel laccase is ozymegenes from Trametes sp. AH28-2 and analyses of their differential expression. Appl Microbiol Biotechnol 71:493–501CrossRefGoogle Scholar
  56. Yang Y, Wei F, Zhuo R, Fan F, Liu H, Zhang C (2013) Enhancing the laccase production and laccase gene expression in the white-rot fungus Trametes velutina 5930 with great potential for biotechnological applications by different metal ions and aromatic compounds. PLoS ONE 8:79307CrossRefGoogle Scholar
  57. Yang J, Wang G, Ng TB, Lin J, Ye X (2016) Laccase production and differential transcription of laccase genes in Cerrena sp. in response to metal ions, aromatic compounds, and nutrients. Front Microbiol 6:1558PubMedPubMedCentralGoogle Scholar
  58. Yoshida H (1883) Chemistry of lacquer (Urusbz) part 1. J Chem SOL 43:472–486CrossRefGoogle Scholar
  59. Yoshimura I, Yamamoto Y, Nakano T, Finnie J (2002) Isolation and culture of lichen photobionts and mycobionts. Protoc Lichens.  https://doi.org/10.1007/978-3-642-56359-1-1 CrossRefGoogle Scholar
  60. Zamboni A, Pierantoni L, Franceschi P (2008) de Total RNA extraction from strawberry tree (Arbutus unedo) and several other woody-plants. J Biogeosci For Bologna 1(1):122–125Google Scholar
  61. Zavarzina AG, Zavarzin AA (2006) Laccase and tyrosinase activities in lichens. Microbiol 75:1–12CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  • Elif Değerli
    • 1
  • Sevcan Yangın
    • 1
  • Demet Cansaran-Duman
    • 1
    Email author
  1. 1.System Biotechnology Advance Research Unit, Biotechnology InstituteAnkara UniversityAnkaraTurkey

Personalised recommendations