CoChat
Sign Up
Cited by 515

The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.

Laccases: structure, function, and potential application in water bioremediation

Arregui, Leticia, Ayala, Marcela, Gómez-Gil, Ximena, Gutiérrez-Soto, Guadalupe, Hernández-Luna, Carlos Eduardo, Herrera de los Santos, Mayra, Levin, Laura, Rojo-Domínguez, Arturo, Romero-Martínez, Daniel, Saparrat, Mario C. N., Trujillo-Roldán, Mauricio A., Valdez-Cruz, Norma A.·2019·Microbial Cell Factories
DOI 10.1186/s12934-019-1248-0PMC PMC6854816
Open this paper in CoChat — free account

Abstract

The global rise in urbanization and industrial activity has led to the production and incorporation of foreign contaminant molecules into ecosystems, distorting them and impacting human and animal health. Physical, chemical, and biological strategies have been adopted to eliminate these contaminants from water bodies under anthropogenic stress. Biotechnological processes involving microorganisms and enzymes have been used for this purpose; specifically, laccases, which are broad spectrum biocatalysts, have been used to degrade several compounds, such as those that can be found in the effluents from industries and hospitals. Laccases have shown high potential in the biotransformation of diverse pollutants using crude enzyme extracts or free enzymes. However, their application in bioremediation and water treatment at a large scale is limited by the complex composition and high salt concentration and pH values of contaminated media that affect protein stability, recovery and recycling. These issues are also associated with operational problems and the necessity of large-scale production of laccase. Hence, more knowledge on the molecular characteristics of water bodies is required to identify and develop new laccases that can be used under complex conditions and to develop novel strategies and processes to achieve their efficient application in treating contaminated water. Recently, stability, efficiency, separation and reuse issues have been overcome by the immobilization of enzymes and development of novel biocatalytic materials. This review provides recent information on laccases from different sources, their structures and biochemical properties, mechanisms of action, and application in the bioremediation and biotransformation of contaminant molecules in water. Moreover, we discuss a series of improvements that have been attempted for better organic solvent tolerance, thermo-tolerance, and operational stability of laccases, as per process requirements.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s12934-019-1248-0

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Figures

Fig. 1 Schematic illustration of the potential sources of water contaminants and their bioremediation by laccases. Emerging contaminants such as antibiotics, endocrine disruptors, dye-based pollutants and pharmaceutical drugs are often released into the environment causing harmful impacts and health problems to humans and other animals, water treatment with laccases and their biotechnological approaches generate less-toxic, inert or fully degraded compounds
Fig. 1 Schematic illustration of the potential sources of water contaminants and their bioremediation by laccases. Emerging contaminants such as antibiotics, endocrine disruptors, dye-based pollutants and pharmaceutical drugs are often released into the environment causing harmful impacts and health problems to humans and other animals, water treatment with laccases and their biotechnological approaches generate less-toxic, inert or fully degraded compoundsCC BY · PubMed Central
Fig. 2 Phylogenetic tree constructed with some of the different organism sources of laccases, as well as some of their applications in bioremediation. According to their bacterial, insect, plant or fungal origin, they are colored with blue, red, green or orange, respectively. The alignments and phylogenetic relationships were done using the MEGA X suite
Fig. 2 Phylogenetic tree constructed with some of the different organism sources of laccases, as well as some of their applications in bioremediation. According to their bacterial, insect, plant or fungal origin, they are colored with blue, red, green or orange, respectively. The alignments and phylogenetic relationships were done using the MEGA X suiteCC BY · PubMed Central
Fig. 3 Cartoon structures of the three-domain laccase from Bacillus subtilis (PDB 1GSK) and the homotrimeric two-domain laccase from Streptomyces coelicolor (PDB 3CG8). The domain assignations were made using the SWORD partition algorithm
Fig. 3 Cartoon structures of the three-domain laccase from Bacillus subtilis (PDB 1GSK) and the homotrimeric two-domain laccase from Streptomyces coelicolor (PDB 3CG8). The domain assignations were made using the SWORD partition algorithmCC BY · PubMed Central
Fig. 4 Representation of the different amino acids of the catalytic site that coordinates the catalytic coppers in Trametes versicolor laccase (PDB 1KYA). The amino acids of the histidine-cysteine pathway are in green
Fig. 4 Representation of the different amino acids of the catalytic site that coordinates the catalytic coppers in Trametes versicolor laccase (PDB 1KYA). The amino acids of the histidine-cysteine pathway are in greenCC BY · PubMed Central
Fig. 5 Laccase structure conservation and function. a Structure of Trametes versicolor (PDB ID 1GYC), and Bacillus subtilis (PDB ID 1GSK) laccases compared to Cucurbita pepo (zucchini) ascorbate oxidase (PDB ID 1AOZ) from left to right. Domain 1 (D1) is at the front and right of the structure, domain 2 (D2) is behind and in the upper portion, domain 3 (D3) is at the left. Brown spheres symbolize the position of copper atoms, T1 above the trinuclear cluster. b The molecular surface shows protruding chemical groups, in red, and concave or cavity regions, in green. Some of these latter regions correspond to the ligand-binding site (LB) along with the dioxygen molecule entrance (O2) and the water exit (H2O) channels. Central and right images were created from that on the left by rotating it 30° over the horizontal axis, or 30° over the vertical axis, respectively
Fig. 5 Laccase structure conservation and function. a Structure of Trametes versicolor (PDB ID 1GYC), and Bacillus subtilis (PDB ID 1GSK) laccases compared to Cucurbita pepo (zucchini) ascorbate oxidase (PDB ID 1AOZ) from left to right. Domain 1 (D1) is at the front and right of the structure, domain 2 (D2) is behind and in the upper portion, domain 3 (D3) is at the left. Brown spheres symbolize the position of copper atoms, T1 above the trinuclear cluster. b The molecular surface shows protruding chemical groups, in red, and concave or cavity regions, in green. Some of these latter regions correspond to the ligand-binding site (LB) along with the dioxygen molecule entrance (O2) and the water exit (H2O) channels. Central and right images were created from that on the left by rotating it 30° over the horizontal axis, or 30° over the vertical axis, respectivelyCC BY · PubMed Central
Fig. 6 Mechanism, kinetic model and structural elements involved in laccase functional properties and reaction. a Representation of the laccase mechanism of action in the active site of Trametes versicolor laccase (PDB 1KYA). In orange are represented those aminoacids involved in the binding, stabilization and orientation of the substrate, in grey and green those that are involved in the coordination of catalytic coppers and the electron transfer and in yellow those that transfer protons for the oxygen assisted reduction. b Laccase action on a lignin-model illustrating the domino effect [198]. c Complex two-site ping-pong bi-bi kinetic model proposed for the laccase reaction [184, 185]. d Structural and functional elements involved in different steps of the laccase reaction
Fig. 6 Mechanism, kinetic model and structural elements involved in laccase functional properties and reaction. a Representation of the laccase mechanism of action in the active site of Trametes versicolor laccase (PDB 1KYA). In orange are represented those aminoacids involved in the binding, stabilization and orientation of the substrate, in grey and green those that are involved in the coordination of catalytic coppers and the electron transfer and in yellow those that transfer protons for the oxygen assisted reduction. b Laccase action on a lignin-model illustrating the domino effect [198]. c Complex two-site ping-pong bi-bi kinetic model proposed for the laccase reaction [184, 185]. d Structural and functional elements involved in different steps of the laccase reactionCC BY · PubMed Central

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Research works printed but not linked: 205

  1. Daughton CG. Non-regulated water contaminants: emerging research. Environ Impact Assess Rev. 2004;24:711–32. https://doi.org/10.1016/j.eiar.2004.06.003. · DOI
  2. Cabana H, Jiwan JLH, Rozenberg R, Elisashvili V, Penninckx M, Agathos SN, Jones JP. Elimination of endocrine disrupting chemicals nonylphenol and bisphenol A and personal care product ingredient triclosan using enzyme preparation from the white rot fungus Coriolopsis polyzona. Chemosphere. 2007;67:770–8. https://doi.org/10.1016/j.chemosphere.2006.10.037. · DOI
  3. Chakroun H, Mechichi T, Martinez MJ, Dhouib A, Sayadi S. Purification and characterization of a novel laccase from the ascomycete Trichoderma atroviride: application on bioremediation of phenolic compounds. Process Biochem. 2010;45:507–13. https://doi.org/10.1016/j.procbio.2009.11.009. · DOI
  4. Corcoran E, Nellemann C, Baker E, Bos R, Osborn D, Savelli H. Sick water? The central role of wastewater management in sustainable development. A rapid response assessment. United Nations Environment Programme: Nairobi; 2010. ISBN 978-82-7701-075-5.
  5. Bilal M, Asgher M, Parra-Saldivar R, Hu H, Wang W, Zhang X, Iqbal HMN. Immobilized ligninolytic enzymes: an innovative and environmental responsive technology to tackle dye-based industrial pollutants—a review. Sci Total Environ. 2017;576:646–59. https://doi.org/10.1016/j.scitotenv.2016.10.137. · DOI · Paper page
  6. Klaper R, Welch LC. Emerging contaminant threats and the Great Lakes: existing science, estimating relative risk and determining policies. Chicago: Alliance for the Great Lakes; 2011.
  7. Garcia-Morales R, Rodríguez-Delgado M, Gomez-Mariscal K, Orona-Navar C, Hernandez-Luna C, Torres E, Parra R, Cárdenas-Chávez D, Mahlknecht J, Ornelas-Soto N. Biotransformation of endocrine-disrupting compounds in groundwater: bisphenol A, nonylphenol, ethynylestradiol and triclosan by a laccase cocktail from Pycnoporus sanguineus CS43. Water Air Soil Pollut. 2015;226:251. https://doi.org/10.1007/s11270-015-2514-3. · DOI
  8. Nguyen LN, Hai FI, Price WE, Leusch FD, Roddick F, McAdam EJ, Magram SF, Nghiem LD. Continuous biotransformation of bisphenol A and diclofenac by laccase in an enzymatic membrane reactor. Int Biodeter Biodegr. 2014;95:25–32. https://doi.org/10.1016/j.ibiod.2014.05.017. · DOI
  9. Gasser CA, Ammann EM, Shahgaldian P, Corvini PFX. Laccases to take on the challenge of emerging organic contaminants in wastewater. Appl Microbiol Biotechnol. 2014;98:9931–52. https://doi.org/10.1007/s00253-014-6177-6. · DOI
  10. Rodríguez-Delgado M, Orona-Navar C, García-Morales R, Hernandez-Luna C, Parra R, Mahlknecht J, Ornelas-Soto N. Biotransformation kinetics of pharmaceutical and industrial micropollutants in groundwaters by a laccase cocktail from Pycnoporus sanguineus CS43 fungi. Int Biodeter Biodegr. 2016;108:34–41. https://doi.org/10.1016/j.ibiod.2015.12.003. · DOI
  11. Spina F, Cordero C, Schilirò T, Sgorbini B, Pignata C, Gilli G, Bicci C, Varese GC. Removal of micropollutants by fungal laccases in model solution and municipal wastewater: evaluation of estrogenic activity and ecotoxicity. J Clean Prod. 2015;100:185–94. https://doi.org/10.1016/j.jclepro.2015.03.047. · DOI
  12. Deblonde T, Cossu-Leguille C, Hartemann P. Emerging pollutants in wastewater: a review of the literature. Int J Hyg Environ Health. 2011;214:442–8. https://doi.org/10.1016/j.ijheh.2011.08.002. · DOI
  13. Chatha SAS, Asgher M, Iqbal HMN. Enzyme-based solutions for textile processing and dye contaminant biodegradation—a review. Environ Sci Pollut Res Int. 2017;24:14005–18. https://doi.org/10.1007/s11356-017-8998-1. · DOI
  14. Barber LB, Loyo-Rosales JE, Rice CP, Minarik TA, Oskouie AK. Endocrine disrupting alkylphenolic chemicals and other contaminants in wastewater treatment plant effluents, urban streams, and fish in the Great Lakes and upper Mississippi River Regions. Sci Total Environ. 2015;517:195–206. https://doi.org/10.1016/j.scitotenv.2015.02.035. · DOI
  15. Giardina P, Faraco V, Pezzella C, Piscitelli A, Vanhulle S, Sannia G. Laccases: a never-ending story. Cell Mol Life Sci. 2010;67:69–385. https://doi.org/10.1007/s00018-009-0169-1. · DOI · Paper page
  16. Riva S. Laccases: blue enzymes for green chemistry. Trends Biotechnol. 2016;24:219–26. https://doi.org/10.1016/j.tibtech.2006.03.006. · DOI
  17. Kim C, Lorenz WW, Hoopes JT, Dean JF. Oxidation of phenolate siderophores by the multicopper oxidase encoded by the Escherichia coli yacK gene. J Bacteriol. 2001;183:4866–75. https://doi.org/10.1128/JB.183.16.4866-4875.2001. · DOI
  18. Morozova OV, Shumakovich GP, Shleev SV, Yaropolov YI. Laccase-mediator systems and their applications: a review. Appl Biochem Microbiol. 2007;43:523–35. https://doi.org/10.1134/S0003683807050055. · DOI
  19. Upadhyay P, Shrivastava R, Agrawal PK. Bioprospecting and biotechnological applications of fungal laccase. 3 Biotech. 2016;6:15. https://doi.org/10.1007/s13205-015-0316-3. · DOI · Paper page
  20. Mayer AM, Staples RC. Laccase: new functions for an old enzyme. Phytochemistry. 2002;60:551–65. https://doi.org/10.1016/S0031-9422(02)00171-1. · DOI
  21. Santhanam N, Vivanco JM, Decker SR, Reardon KF. Expression of industrially relevant laccases: prokaryotic style. Trends Biotechnol. 2011;29:480–9. https://doi.org/10.1016/j.tibtech.2011.04.005. · DOI
  22. Mate DM, Alcalde M. Laccase engineering: from rational design to directed evolution. Biotechnol Adv. 2015;33:25–40. https://doi.org/10.1016/j.biotechadv.2014.12.007. · DOI
  23. Viswanath B, Rajesh B, Janardhan A, Kumar AP, Narasimha G. Fungal laccases and their applications in bioremediation. Enzyme Res. 2014;2014:1–21. https://doi.org/10.1155/2014/163242. · DOI
  24. Bertrand G. Sur la presence simultanee de la laccase et de la tyrosinase dans le suc de quelques champignons. CR Hebd Seances Acad Sci. 1896;123:463–5.
  25. Strong P, Claus H. Laccase: a review of its past and its future in bioremediation. Crit Rev Environ Sci Technol. 2011;41:373–434. https://doi.org/10.1080/10643380902945706. · DOI
  26. Kiliç N, Nasiri F, Cansaran-Duman D. Fungal laccase enzyme applications in bioremediation of polluted wastewater. Phytoremediation. New York: Springer; 2016. p. 201–9.
  27. Thurston CF. The structure and function of fungal laccases. Microbiology. 1994;140:19–26. https://doi.org/10.1099/13500872-140-1-19. · DOI · Paper page
  28. Alcalde M. Laccases: biological functions, molecular structure and industrial applications. In: Polaina J, MacCabe A, editors. Industrial enzymes: structure, function and applications. Dordrecht: Springer; 2007. p. 461–76. ISBN 978-1-4020-5377-1. · DOI
  29. Baldrian P. Fungal laccases–occurrence and properties. FEMS Microbiol Rev. 2006;30:215–42. https://doi.org/10.1111/j.1574-4976.2005.00010.x. · DOI
  30. Rivera-Hoyos CM, Morales-Álvarez ED, Poutou-Piñales RA, Pedroza-Rodríguez AM, RodrÍguez-Vázquez R, Delgado-Boada JM. Fungal laccases. Fungal Biol Rev. 2013;27:67–82. https://doi.org/10.1016/j.fbr.2013.07.001. · DOI · Paper page
  31. Maestre-Reyna M, Liu WC, Jeng WY, Lee CC, Hsu CA, Wen TN, Wang AHJ, Shyur LF. Structural and functional roles of glycosylation in fungal laccase from Lentinus sp. PLoS ONE. 2015;10:e0120601. https://doi.org/10.1371/journal.pone.0120601. · DOI
  32. Shleev SV, Morozova OV, Nikitina OV, Gorshina ES, Rusinova TV, Serezhenkov VA, Burbaev DS, Gazaryan IG, Yaropolov AI. Comparison of physico-chemical characteristics of four laccases from different basidiomycetes. Biochimie. 2004;86:693–710. https://doi.org/10.1016/j.biochi.2004.08.005. · DOI
  33. Rodgers CJ, Blanford CF, Giddens SR, Skamnioti P, Armstrong FA, Gurr SJ. Designer laccases: a vogue for high-potential fungal enzymes? Trends Biotechnol. 2010;28:63–72. https://doi.org/10.1016/j.tibtech.2009.11.001. · DOI
  34. Maté D, García-Ruiz E, Camarero S, Alcalde M. Directed evolution of fungal laccases. Curr Genom. 2011;12:113–22. https://doi.org/10.2174/138920211795564322. · DOI
  35. Agrawal K, Chaturvedi V, Verma P. Fungal laccase discovered but yet undiscovered. Bioresour Bioprocess. 2018;5:4. https://doi.org/10.1186/s40643-018-0190-z. · DOI
  36. Kuramitz H, Saitoh J, Hattori T, Tanaka S. Electrochemical removal of p-nonylphenol form dilute solutions using a carbon fiber anode. Water Res. 2002;36:3323–9. https://doi.org/10.1016/S0043-1354(02)00040-4. · DOI
  37. Tavares APM, Cristóvão RO, Gamelas JAF, Loureiro JM, Boaventura RAR, Macedo EA. Sequential decolourization of reactive textile dyes by laccaase mediator system. J Chem Technol Biotechnol. 2009;84:442–6. https://doi.org/10.1002/jctb.2060. · DOI
  38. Acevedo F, Pizzul L, del Pilar Castillo M, Cuevas R, Diez MC. Degradation of polycyclic aromatic hydrocarbons by the Chilean white-rot fungus Anthracophyllum discolor. J Hazard Mater. 2011;185:212–9. https://doi.org/10.1016/j.jhazmat.2010.09.020. · DOI
  39. Uribe-Alvarez C, Ayala M, Perezgasga L, Naranjo L, Urbina H, Vazquez-Duhalt R. First evidence of mineralization of petroleum asphaltenes by a strain of Neosartorya fischeri. Microb Biotechnol. 2011;4:663–72. https://doi.org/10.1111/j.1751-7915.2011.00269.x. · DOI
  40. Ramírez-Cavazos LI, Junghanns C, Ornelas-Soto N, Cárdenas-Chávez DL, Hernández-Luna C, Demarche P, Enaud E, García-Morales R, Agathos SN, Parra R. Purification and characterization of two thermostable laccases from Pycnoporus sanguineus and potential role in degradation of endocrine disrupting chemicals. J Mol Cat B Enzym. 2014;108:32–42. https://doi.org/10.1016/j.molcatb.2014.06.006. · DOI
  41. Barrios-Estrada C, de Jesús Rostro-Alanis M, Parra AL, Belleville MP, Sanchez-Marcano J, Iqbal HM, Parra-Saldívar R. Potentialities of active membranes with immobilized laccase for bisphenol A degradation. Int J Biol Macromol. 2018;108:837–44. https://doi.org/10.1016/j.ijbiomac.2017.10.177. · DOI
  42. Carabajal M, Perullini M, Jobbágy M, Ullrich R, Hofrichter M, Levin L. Removal of phenol by immobilization of Trametes versicolor in silica–alginate–fungus biocomposites and loofa sponge. CLEAN Soil Air Water. 2016;44:180–8. https://doi.org/10.1002/clen.201400366. · DOI
  43. Gaitan IJ, Medina SC, González JC, Rodríguez A, Espejo ÁJ, Osma JF, Sarria V, Alméciga-Díaz CJ, Sánchez OF. Evaluation of toxicity and degradation of a chlorophenol mixture by the laccase produced by Trametes pubescens. Bioresour Technol. 2011;102:3632–5. https://doi.org/10.1016/j.biortech.2010.11.040. · DOI
  44. Kunamneni A, Ghazi I, Camarero S, Ballesteros A, Plou FJ, Alcalde M. Decolorization of synthetic dyes by laccase immobilized on epoxy-activated carriers. Process Biochem. 2008;43:169–78. https://doi.org/10.1016/j.procbio.2007.11.009. · DOI · Paper page
  45. Simões MF, Maiorano AE, dos Santos JG, Peixoto L, de Souza RFB, Neto AO, Brito AG, Ottoni CA. Microbial fuel cell-induced production of fungal laccase to degrade the anthraquinone dye remazol brilliant blue R. Environ Chem Lett. 2019. https://doi.org/10.1007/s10311-019-00876-y. · DOI
  46. Palazzolo MA, Postemsky PD, Kurina-Sanz M. From agro-waste to tool: biotechnological characterization and application of Ganoderma lucidum E47 laccase in dye decolorization. 3 Biotech. 2019;9(6):213. https://doi.org/10.1007/s13205-019-1744-2. · DOI
  47. Iark D, dos Reis Buzzo AJ, Garcia JAA, Côrrea VG, Helm CV, Corrêa RCG, Peralta RA, Moreira RFPM, Bracht A, Peralta RM. Enzymatic degradation and detoxification of azo dye Congo red by a new laccase from Oudemansiella canarii. Bioresour Technol. 2019. https://doi.org/10.1016/j.biortech.2019.121655. · DOI
  48. Garcia LF, Lacerda MF, Thomaz DV, de Souza JC, Pereira M, de Souza G, Schimidt F, Santiago MF. Optimization of laccase-alginate-chitosan-based matrix toward 17 α-ethinylestradiol removal. Prep Biochem Biotechnol. 2019;49:375–83. https://doi.org/10.1080/10826068.2019.1573195. · DOI
  49. Alharbi SK, Nghiem LD, van de Merwe JP, Leusch FD, Asif MB, Hai FI, Price WE. Degradation of diclofenac, trimethoprim, carbamazepine, and sulfamethoxazole by laccase from Trametes versicolor: transformation products and toxicity of treated effluent. Biocatal Biotransform. 2019. https://doi.org/10.1080/10242422.2019.1580268. · DOI
  50. Pulicharla R, Das RK, Brar SK, Drogui P, Surampalli RY. Degradation kinetics of chlortetracycline in wastewater using ultrasonication assisted laccase. Chem Eng J. 2018;347:828–35. https://doi.org/10.1016/j.cej.2018.04.162. · DOI
  51. Singh SK, Khajuria R, Kaur L. Biodegradation of ciprofloxacin by white rot fungus Pleurotus ostreatus. 3 Biotech. 2017;7(1):69. https://doi.org/10.1007/s13205-017-0684-y. · DOI
  52. Navada KK, Kulal A. Enzymatic degradation of chloramphenicol by laccase from Trametes hirsuta and comparison among mediators. Int Biodeter Biodegr. 2019;138:63–9. https://doi.org/10.1016/j.ibiod.2018.12.012. · DOI
  53. Fukuda T, Uchida H, Takashima Y, Uwajima T, Kawabata T, Suzuki M. Degradation of bisphenol A by purified laccase from Trametes villosa. Biochem Biophys Res Commun. 2001;284:704–6. https://doi.org/10.1006/bbrc.2001.502. · DOI
  54. Becker D, Rodriguez-Mozaz S, Insa S, Schoevaart R, Barcelo D, de Cazes M, Belleville MP, Sanchez-Marcano J, Misovic A, Oehlmann J, Wagner M. Removal of endocrine disrupting chemicals in wastewater by enzymatic treatment with fungal laccases. Org Process Res Dev. 2017;21(4):480–91. https://doi.org/10.1021/acs.oprd.6b00361. · DOI
  55. Golveia JCS, Santiago MF, Sales PTF, Sartoratto A, Ponezi AN, Thomaz DV, Gil ES, Bara MTF. Cupuaçu (Theobroma grandiflorum) residue and its potential application in the bioremediation of 17-Α-ethinylestradiol as a Pycnoporus sanguineus laccase inducer. Prep Biochem Biotechnol. 2018;48(6):541–8. https://doi.org/10.1080/10826068.2018.1466161. · DOI
  56. Casas N, Parella T, Vicent T, Caminal G, Sarrà M. Metabolites from the biodegradation of triphenylmethane dyes by Trametes versicolor or laccase. Chemosphere. 2009;75(10):1344–9. https://doi.org/10.1016/j.chemosphere.2009.02.029. · DOI
  57. Grassi E, Scodeller P, Filiel N, Carballo R, Levin L. Potential of Trametes trogii culture fluids and its purified laccase for the decolorization of different types of recalcitrant dyes without the addition of redox mediators. Int Biodeter Biodegr. 2011;65:635–43. https://doi.org/10.1016/j.ibiod.2011.03.007. · DOI
  58. Piscitelli A, Pezzella C, Giardina P, Faraco V, Sannia G. Heterologous laccase production and its role in industrial applications. Bioeng Bugs. 2010;1:254–64. https://doi.org/10.4161/bbug.1.4.11438. · DOI
  59. Salony GN, Baranwal R, Chhabra M, Mishra S, Chaudhuri TK, Bisaria VS. Laccase of Cyathus bulleri: structural, catalytic characterization and expression in Escherichia coli. Biochim Biophys Acta. 2008;1784:259–68. https://doi.org/10.1016/j.bbapap.2007.11.006. · DOI
  60. Klonowska A, Gaudin C, Asso M, Fournel A, Reglier M, Tron T. LAC3, a new low redox potential laccase from Trametes sp. strain C30 obtained as a recombinant protein in yeast. Enzyme Microb Technol. 2005;36:34–41. https://doi.org/10.1016/j.enzmictec.2004.03.022. · DOI
  61. Colao MC, Lupino S, Garzillo AM, Buonocore V, Ruzzi M. Heterologous expression of lcc1 gene from Trametes trogii in Pichia pastoris and characterization of the recombinant enzyme. Microb Cell Fact. 2006;5:31. https://doi.org/10.1186/1475-2859-5-31. · DOI
  62. Madzak C, Otterbein L, Chamkha M, Moukha S, Asther M, Gaillardin C, Beckerich JM. Heterologous production of a laccase from the basidiomycete Pycnoporus cinnabarinus in the dimorphic yeast Yarrowia lipolytica. FEMS Yeast Res. 2005;5:635–46. https://doi.org/10.1016/j.femsyr.2004.10.009. · DOI
  63. Pardo I, Rodríguez-Escribano D, Aza P, De Salas F, Martínez AT, Camarero S. A highly stable laccase obtained by swapping the second cupredoxin domain. Sci Rep. 2018;8:15669. https://doi.org/10.1038/s41598-018-34008-3. · DOI
  64. Yaver DS, Xu F, Golightly EJ, Brown KM, Brown SH, Rey MW, Schneider P, Halkier T, Mondorf K, Dalboge H. Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Appl Environ Microbiol. 1996;62:834–41. · DOI
  65. Bohlin C, Jönsson LJ, Roth R, Van Zyl WH. Heterologous expression of Trametes versicolor laccase in Pichia pastoris and Aspergillus niger. Appl Biochem Biotechnol. 2006;129–132:195–214. https://doi.org/10.1007/978-1-59745-268-7_15. · DOI
  66. Balcázar-López E, Méndez-Lorenzo LH, Batista-García RA, Esquivel-Naranjo U, Ayala M, Kumar VV, Savary O, Cabana H, Herrera-Estrella A, Folch-Mallol JL. Xenobiotic compounds degradation by heterologous expression of a Trametes sanguineus laccase in Trichoderma atroviride. PLoS ONE. 2016;11:e0147997. https://doi.org/10.1371/journal.pone.0147997. · DOI
  67. Wang B, Yan Y, Xu J, Fu X, Han H, Gao J, Li Z, Wang L, Tian Y, Peng R. Heterologous expression and characterization of a laccase from Laccaria bicolor in Pichia pastoris and Arabidopsis thaliana. J Microbiol Biotechnol. 2018;28:2057–63. https://doi.org/10.1080/13102818.2015.1104261. · DOI
  68. Bailey MR, Woodard SL, Callaway E, Beifuss K, Magallanes-Lundback M, Lane JR, Horn ME, Mallubhotla H, Delaney DD, Ward M, Van Gastel F, Howard JA, Hood EE. Improved recovery of active recombinant laccase from maize seed. Appl Microb Biotechnol. 2004;63:390–7. https://doi.org/10.1007/s00253-003-1362-z. · DOI
  69. Campos PA, Levin LN, Wirth SA. Heterologous production, characterization and dye decolorization ability of a novel thermostable laccase isoenzyme from Trametes trogii BAFC 463. Process Biochem. 2016;51:895–903. https://doi.org/10.1016/j.procbio.2016.03.015. · DOI · Paper page
  70. Darvishi F, Moradi M, Jolivalt C, Madzak C. Laccase production from sucrose by recombinant Yarrowia lipolytica and its application to decolorization of environmental pollutant dyes. Ecotox Environ Safe. 2018;165:278–83. https://doi.org/10.1016/j.ecoenv.2018.09.026. · DOI
  71. Yoshida H. Chemistry of lacquer (Urushi) part 1. J Chem Soc. 1883;43:472–86. https://doi.org/10.1039/ct8834300472. · DOI
  72. Frasconi M, Favero G, Boer H, Koivula A, Mazzei F. Kinetic and biochemical properties of high and low redox potential laccases from fungal and plant origin. Biochim Biophys Acta. 2010;1804:899–908. https://doi.org/10.1016/j.bbapap.2009.12.018. · DOI
  73. Sterjiades R, Jeffrey FDD, Eriksson KEL. Laccase from sycamore maple (Acer pseudoplatanus) polymerizes monolignols. Plant Physiol. 1992;99:1162–8. https://doi.org/10.1104/pp.99.3.1162. · DOI
  74. Zhao Q, Nakashima J, Chen F, Yin YB, Fu CX, Yun JF, Shao H, Wang XQ, Wang ZY, Dixon RA. Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell. 2013;25:3976–87. https://doi.org/10.1105/tpc.113.117770. · DOI
  75. Tobimatsu Y, Schuetz M. Lignin polymerization: how do plants manage the chemistry so well? Curr Opin Biotechnol. 2019;56:75–81. https://doi.org/10.1016/j.copbio.2018.10.001. · DOI
  76. Liang M, Davis E, Gardner D, Cai X, Wu Y. Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta. 2006;224:1185–96. https://doi.org/10.1007/s00425-006-0300. · DOI
  77. Nigam D, Kavita P, Tripathi RK, Ranjan A, Goel R, Asif M, Shukla A, Singh G, Rana D, Sawant SV. Transcriptome dynamics during fibre development in contrasting genotypes of Gossypium hirsutum L. Plant Biotechnol J. 2014;12:204–18. https://doi.org/10.1111/pbi.12129. · DOI
  78. Balasubramanian VK, Rai KM, Thu SW, Hii MM, Mendu V. Genome-wide identification of multifunctional laccase gene family in cotton (Gossypium spp.); expression and biochemical analysis during fiber development. Sci Rep. 2016;6:34309. https://doi.org/10.1038/srep34309. · DOI
  79. Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V, Torabinejad J, Wu Y. Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot. 2006;57:2563–9. https://doi.org/10.1093/jxb/erl022. · DOI
  80. Cho HY, Lee C, Hwang SG, Park YC, Lim HL, Jang CS. Overexpression of the OsChI1 gene, encoding a putative laccase precursor, increases tolerance to drought and salinity stress in transgenic Arabidopsis. Gene. 2014;552:98–105. https://doi.org/10.1016/j.gene.2014.09.018. · DOI
  81. Liu Q, Luo L, Wang X, Shen Z, Zheng L. Comprehensive analysis of rice laccase gene (OsLAC) family and ectopic expression of OsLAC10 enhances tolerance to copper stress in Arabidopsis. Int J Mol Sci. 2017;18:209. https://doi.org/10.3390/ijms18020209. · DOI
  82. Wang GD, Li QJ, Luo B, Chen XY. Ex planta phytoremediation of trichlorophenol and phenolic allelo chemicals via an engineered secretory laccase. Nat Biotechnol. 2004;22:893–7. https://doi.org/10.1038/nbt982. · DOI
  83. Watharkar AD, Kadam SK, Khandare RV, Kolekar PD, Jeon BH, Jadhav JP, Govindwar SP. Asparagus densiflorus in a vertical subsurface flow phytoreactor for treatment of real textile effluent: a lab to land approach for in situ soil remediation. Ecotoxicol Environ Saf. 2018;161:70–7. https://doi.org/10.1016/j.ecoenv.2018.05.078. · DOI
  84. Kagalkar AN, Khandare RV, Govindwar SP. Textile dye degradation potential of plant laccase significantly enhances upon augmentation with redox mediators. RSC Adv. 2015;5:80505–17. https://doi.org/10.1039/c5ra12454a. · DOI
  85. Telke AA, Kagalkar AN, Jagtap UB, Desai NS, Bapat VA, Govidwar SP. Biochemical characterization of laccase from hairy root culture of Brassica juncea L. and role of redox mediators to enhance its potential for the decolorization of textile dyes. Planta. 2011;234:1137–49. https://doi.org/10.1007/s00425-011-1469-x. · DOI
  86. Kabra AN, Khandare RV, Kurade MB, Govindwar SP. Phytoremediation of a sulphonated azo dye Green HE4B by Glandularia pulchella (Sweet) Tronc. (Moss Verbena). Environ Sci Pollut Res Int. 2011;18:1360–73. https://doi.org/10.1007/s11356-011-0491-7. · DOI
  87. Rane NR, Chandanshive VV, Watharkar AD, Khandare RV, Patil TS, Pawar PK, Govindwar SP. Phytoremediation of sulfonated Remazol Red dye and textile effluents by Alternanthera philoxeroides: an anatomical, enzymatic and pilot scale study. Water Res. 2015;83:271–81. https://doi.org/10.1016/j.watres.2015.06.046. · DOI
  88. Chandanshive VV, Kadam SK, Khandare RV, Kurade MB, Jeon BH, Jadhav JP, Govindwar SP. In situ phytoremediation of dyes from textile wastewater using garden ornamental plants, effect on soil quality and plant growth. Chemosphere. 2018;210:968–76. https://doi.org/10.1016/j.chemosphere.2018.07.064. · DOI
  89. Huang MT, Lu YC, Zhang S, Luo F, Yang H. Rice (Oryza sativa) laccases involved in modification and detoxification of herbicides atrazine and isoproturon residues in plants. J Agric Food Chem. 2016;64:6397–406. https://doi.org/10.1021/acs.jafc.6b02187. · DOI
  90. Chiaiese P, Palomba F, Galante C, Esposito S, de Biasi MG, Filippone E. Transgenic tobacco plants expressing a fungal laccase are able to reduce phenol content from olive mill wastewaters. Int J Phytoremediat. 2012;14:835–44. https://doi.org/10.1080/15226514.2011.628715. · DOI
  91. de Wilde C, Uzan E, Zhou Z, Kruus K, Andberg M, Buchert J, Record E, Asther M, Lomascolo A. Transgenic rice as a novel production system for Melanocarpus and Pycnoporus laccases. Transgenic Res. 2008;17:515–27. https://doi.org/10.1007/s11248-007-9124-9. · DOI
  92. Sonoki T, Kajita S, Ikeda S, Uesugi M, Tatsumi K, Katayama Y, Iimura Y. Transgenic tobacco expressing fungal laccase promotes the detoxification of environmental pollutants. Appl Microb Biotechnol. 2005;67:138–42. https://doi.org/10.1007/s00253-004-1770-8. · DOI
  93. De-Jesús-García R, Folch-Mallol JL, Dubrovsky JG. Transgenic callus of Nicotiana glauca stably expressing a fungal laccase maintains its growth in presence of organic contaminants. Plant Cell Tissue Organ Cult. 2019;138(2):311–24. https://doi.org/10.1007/s11240-019-01626-2. · DOI
  94. Du MH, Yan ZW, Hao YJ, Yan ZT, Si FL, Chen B, Qiao L. Suppression of Laccase 2 severely impairs cuticle tanning and pathogen resistance during the pupal metamorphosis of Anopheles sinensis (Diptera: Culicidae). Parasites Vectors. 2017;10(1):171. https://doi.org/10.1186/s13071-017-2118-4. · DOI
  95. Dittmer NT, Kanost MR. Insect multicopper oxidases: diversity, properties, and physiological roles. Insect Biochem Mol Biol. 2010;40:179–88. https://doi.org/10.1016/j.ibmb.2010.02.006. · DOI
  96. Givaudan A, Effosse A, Faure D, Bouillant M-L, Bally R, Potier P. Polyphenol oxidase in Azospirillum lipoferum isolated from rice rhizosphere: evidence for laccase activity in non-motile strains of Azospirillum lipoferum. FEMS Microbiol Lett. 1993;108:205–10. https://doi.org/10.1111/j.1574-6968.1993.tb06100.x. · DOI
  97. Liu Y, Huang L, Guo W, Jia L, Fu Y, Gui S, Lu F. Cloning, expression, and characterization of a thermostable and pH-stable laccase from Klebsiella pneumoniae and its application to dye decolorization. Process Biochem. 2017;53:125–34. https://doi.org/10.1016/j.procbio.2016.11.015. · DOI
  98. Singh G, Bhalla A, Kaur P, Capalash N, Sharma P. Laccase from prokaryotes: a new source for an old enzyme. Rev Environ Sci Biotechnol. 2011;10:309–26. https://doi.org/10.1007/s11157-011-9257-4. · DOI
  99. Uthandi S, Saad B, Humbard MA, Maupin-Furlow JA. LccA, an archaeal laccase secreted as a highly stable glycoprotein into the extracellular medium by Haloferax volcanii. Appl Environ Microbiol. 2010;76:733–43. https://doi.org/10.1128/AEM.01757-09. · DOI
  100. Mate DM, Alcalde M. Laccase: a multi-purpose biocatalyst at the forefront of biotechnology. Microb Biotechnol. 2017;10:1457–67. https://doi.org/10.1111/1751-7915.12422. · DOI
  101. Martins LO, Durão P, Brissos V, Lindley PF. Laccases of prokaryotic origin: enzymes at the interface of protein science and protein technology. Cell Mol Life Sci. 2015;72:911–22. https://doi.org/10.1007/s00018-014-1822-x. · DOI
  102. Sondhi S, Sharma P, Saini S, Puri N, Gupta N. Purification and characterization of an extracellular, thermo-alkali-stable, metal tolerant laccase from Bacillus tequilensis SN4. PLoS ONE. 2014;9:1–10. https://doi.org/10.1371/journal.pone.0096951. · DOI
  103. Guan ZB, Liao Q, Wang HR, Chen Y, Liao XR. Bacterial laccases: promising biological green tools for industrial applications. Cell Mol Life Sci. 2018;75:3569–92. https://doi.org/10.1007/s00018-018-2883-z. · DOI
  104. Chauhan PS, Goradia B, Saxena A. Bacterial laccase: recent update on production, properties and industrial applications. 3 Biotech. 2017;7:323. https://doi.org/10.1007/s13205-017-0955-7. · DOI
  105. Enguita FJ, Martins LO, Henriques AO, Carrondo MA. Crystal structure of a bacterial endospore coat component. J Biol Chem. 2003;278:19416–25. https://doi.org/10.1074/jbc.M301251200. · DOI
  106. Roberts SA, Weichsel A, Grass G, Thakali K, Hazzard JT, Tollin G, Rensing C, Montfort WR. Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci. 2002;99:2766–71. https://doi.org/10.1073/pnas.052710499. · DOI
  107. Hakulinen N, Rouvinen J. Three-dimensional structures of laccases. Cell Mol Life Sci. 2015;72:857–68. https://doi.org/10.1007/s00018-014-1827-5. · DOI · Paper page
  108. Majumdar S, Lukk T, Solbiati JO, Bauer S, Nair SK, Gronan JE, Gerlt JA. Roles of small laccases from Streptomyces in lignin degradation. Biochemistry. 2014;53:4047–58. https://doi.org/10.1021/bi500285t. · DOI
  109. Lawton TJ, Sayavedra-Soto LA, Arp DJ, Rosenzweig AC. Crystal structure of a two-domain multicopper oxidase implications for the evolution of multicopper blue proteins. J Biol Chem. 2009;284:10174–80. https://doi.org/10.1074/jbc.M900179200. · DOI
  110. Brander S, Mikkelsen JD, Kepp KP. Characterization of an alkali-and halide-resistant laccase expressed in E. coli: CotA from Bacillus clausii. PLoS ONE. 2014;9:e99402. https://doi.org/10.1371/journal.pone.0099402. · DOI
  111. Songulashvili G, Jimenéz-Tobón GA, Jaspers C, Penninckx MJ. Immobilized laccase of Cerrena unicolor for elimination of endocrine disruptor micropollutants. Fungal Biol. 2012;116:883–9. https://doi.org/10.1016/j.funbio.2012.05.005. · DOI
  112. Trubitsina LI, Tishchenko SV, Gabdulkhakov AG, Lisov AV, Zakharova MV, Leontievsky AA. Structural and functional characterization of two-domain laccase from Streptomyces viridochromogenes. Biochimie. 2015;112:151–9. https://doi.org/10.1016/j.biochi.2015.03.005. · DOI
  113. Jimenez-Juarez N, Baeza A, Roman-Miranda R, Vazquez-Duhalt R, Valderrama B, Sánchez-Amat A. Alkali and halide-resistant catalysis by the multipotent oxidase from Marinomonas mediterranea. J Biotechnol. 2005;117:73–82. https://doi.org/10.1016/j.jbiotec.2005.01.002. · DOI
  114. Dubé E, Shareck F, Hurtubise Y, Daneault C, Beauregard M. Homologous cloning, expression, and characterization of a laccase from Streptomyces coelicolor and enzymatic decolourisation of an indigo dye. Appl Microbiol Biotechnol. 2008;79:597–603. https://doi.org/10.1007/s00253-008-1475-5. · DOI
  115. Ruijssenaars HJ, Hartmans S. A cloned Bacillus halodurans multicopper oxidase exhibiting alkaline laccase activity. Appl Microbiol Biotechnol. 2004;65:177–82. https://doi.org/10.1007/s00253-004-1571-0. · DOI
  116. Guan Z, Song C, Zhang N, Zhou W. Overexpression, characterization, and dye-decolorizing ability of a thermostable, pH-stable, and organic solvent-tolerant laccase from Bacillus pumilus W3. J Mol Catal B Enzym. 2014;101:1–6. https://doi.org/10.1016/j.molcatb.2013.11.009. · DOI
  117. Theerachat M, Guieysse D, Morel S, Remaud-Siméon M, Chulalaksananukul W. Laccases from marine organisms and their applications in the biodegradation of toxic and environmental pollutants: a review. Appl Biochem Biotechnol. 2019;187:583–611. https://doi.org/10.1007/s12010-018-2829-9. · DOI
  118. Callejón S, Sendra R, Ferrer S, Pardo I. Recombinant laccase from Pediococcus acidilactici CECT 5930 with ability to degrade tyramine. PLoS ONE. 2017;12:1–19. https://doi.org/10.1371/journal.pone.0186019. · DOI
  119. Guan Z, Zhang N, Song C. Molecular cloning, characterization and dye-decolorizing ability of a temperature- and pH-stable laccase from Bacillus subtilis X1. Appl Biochem Biotechnol. 2014;172:1147–57. https://doi.org/10.1007/s12010-013-0614-3. · DOI
  120. Ihssen J, Reiss R, Luchsinger R, Thöny-Meyer L, Richter M. Biochemical properties and yields of diverse bacterial laccase-like multicopper oxidases expressed in Escherichia coli. Sci Rep. 2015;5:1–13. https://doi.org/10.1038/srep10465. · DOI
  121. Tonin F, Rosini E, Piubelli L, Sanchez-Amat A, Pollegioni L. Different recombinant forms of polyphenol oxidase A, a laccase from Marinomonas mediterranea. Protein Expr Purif. 2016;123:60–9. https://doi.org/10.1016/j.pep.2016.03.011. · DOI
  122. Zeng J, Zhu Q, Wu Y, Lin X. Oxidation of polycyclic aromatic hydrocarbons using Bacillus subtilis CotA with high laccase activity and copper independence. Chemosphere. 2016;148:1–7. https://doi.org/10.1016/j.chemosphere.2016.01.019. · DOI
  123. Luo Q, Wang KQ, Liao XR, Guan ZB, Chen Y, Cai YJ, Xia J. Functional expression enhancement of Bacillus pumilus CotA-laccase mutant WLF through site-directed mutagenesis. Enzyme Microb Technol. 2018;109:11–9. https://doi.org/10.1016/j.enzmictec.2017.07.013. · DOI
  124. Liu H, Cheng Y, Du B, Tong C, Liang S, Han S, Zheng S, Lin Y. Overexpression of a novel thermostable and chloride-tolerant laccase from Thermus thermophilus SG0.5JP17-16 in Pichia pastoris and its application in synthetic dye decolorization. PLoS ONE. 2015;10:1–14. https://doi.org/10.1371/journal.pone.0119833. · DOI
  125. Lu L, Wang TN, Xu TF, Wang JY, Wang CL, Zhao M. Cloning and expression of thermo-alkali-stable laccase of Bacillus licheniformis in Pichia pastoris and its characterization. Bioresour Technol. 2013;134:81–6. https://doi.org/10.1016/j.biortech.2013.02.015. · DOI
  126. Ma X, Liu L, Li Q, Liu Y, Yi L, Ma L, Zhai C. High-level expression of a bacterial laccase, CueO from Escherichia coli K12 in Pichia pastoris GS115 and its application on the decolorization of synthetic dyes. Enzyme Microb Technol. 2017;103:34–41. https://doi.org/10.1016/j.enzmictec.2017.04.004. · DOI
  127. Argüello JM, Raimunda D, Padilla-Benavides T. Mechanisms of copper homeostasis in bacteria. Front Cell Infect Microbiol. 2013;3:1–14. https://doi.org/10.3389/fcimb.2013.00073. · DOI
  128. Outten FW, Huffman DL, Hale JA, O’Halloran TV. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem. 2001;276:30670–7. https://doi.org/10.1074/jbc.M104122200. · DOI
  129. Rensing C, Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev. 2003;27:197–213. https://doi.org/10.1016/S0168-6445(03)00049-4. · DOI
  130. Durão P, Chen Z, Fernandes AT, Hildebrandt P, Murgida DH, Todorovic S, Pereira MM, Melo EP, Martins LO. Copper incorporation into recombinant CotA laccase from Bacillus subtilis: characterization of fully copper loaded enzymes. J Biol Inorg Chem. 2008;13:183–93. https://doi.org/10.1007/s00775-007-0312-0. · DOI
  131. Mohammadian M, Fathi-Roudsari M, Mollania N, Badoei-Dalfard A, Khajeh K. Enhanced expression of a recombinant bacterial laccase at low temperature and microaerobic conditions: purification and biochemical characterization. J Ind Microbiol Biotechnol. 2010;37:863–9. https://doi.org/10.1007/s10295-010-0734-5. · DOI
  132. Siroosi M, Amoozegar MA, Khajeh K, Dabirmanesh B. Decolorization of dyes by a novel sodium azide-resistant spore laccase from a halotolerant bacterium, Bacillus safensis sp. strain S31. Water Sci Technol. 2018;77(12):2867–75. https://doi.org/10.2166/wst.2018.281. · DOI
  133. Blánquez A, Rodríguez J, Brissos V, Mendes S, Martins LO, Ball AS, Arias ME, Hernández M. Decolorization and detoxification of textile dyes using a versatile Streptomyces laccase-natural mediator system. Saudi J Biol Sci. 2019;26:913–20. https://doi.org/10.1016/j.sjbs.2018.05.020. · DOI
  134. Singh D, Rawat S, Waseem M, Gupta S, Lynn A, Nitin M, Ramchiary N, Sharma KK. Molecular modeling and simulation studies of recombinant laccase from Yersinia enterocolitica suggests significant role in the biotransformation of non-steroidal anti-inflammatory drugs. Biochem Biophys Res Commun. 2016;469:306–12. https://doi.org/10.1016/j.bbrc.2015.11.096. · DOI
  135. Margot J, Bennati-Granier C, Maillard J, Blánquez P, Barry DA, Holliger C. Bacterial versus fungal laccase: potential for micropollutant degradation. AMB Express. 2013;3(1):63. https://doi.org/10.1186/2191-0855-3-63. · DOI
  136. Reda FM, El-Mekkawy RM, Hassan NS. Detoxification and bioremediation of sulfa drugs and synthetic dyes by Streptomyces mutabilis A17 laccase produced in solid state fermentation. J Pure Appl Microbiol. 2019;13(1):85–96. https://doi.org/10.22207/JPAM.13.1.09. · DOI
  137. Blánquez A, Guillén F, Rodríguez J, Arias ME, Hernández M. The degradation of two fluoroquinolone based antimicrobials by SilA, an alkaline laccase from Streptomyces ipomoeae. World J Microbiol Biotechnol. 2016;32(3):52. https://doi.org/10.1007/s11274-016-2032-5. · DOI
  138. Mot A, Silaghi-Dumitrescu R. Laccases: complex architectures for one-electron oxidations. Biochemistry. 2012;77:1395–407. https://doi.org/10.1134/S0006297912120085. · DOI
  139. Claus H. Laccases: structure, reactions, distribution. Micron. 2004;35:93–6. https://doi.org/10.1016/j.micron.2003.10.029. · DOI
  140. Komori H, Miyazaki K, Higuchi Y. X-ray structure of a two-domain type laccase: a missing link in the evolution of multi-copper proteins. FEBS Lett. 2009;583:1189–95. https://doi.org/10.1016/j.febslet.2009.03.008. · DOI
  141. Nakamura K, Kawabata T, Yura K, Go N. Novel types of two-domain multi-copper oxidases: possible missing links in the evolution. FEBS Lett. 2003;553:239–44. https://doi.org/10.1016/S0014-5793(03)01000-7. · DOI
  142. Nakamura K, Go N. Function and molecular evolution of multicopper blue proteins. Cell Mol Life Sci. 2005;62:2050–66. https://doi.org/10.1007/s00018-004-5076-x. · DOI
  143. Vasin A, Klotchenko S, Puchkova L. Phylogenetic analysis of six-domain multi-copper blue proteins. PLoS Curr. 2013;5:1–18. https://doi.org/10.1371/currents.tol.574bcb0f133fe52835911abc4e296141. · DOI
  144. Geng A, Wu J, Xie RR, Li X, Chang FX, Sun JZ. Characterization of a laccase from a wood-feeding termite, Coptotermes formosanus. Insect Sci. 2016;25:251–8. https://doi.org/10.1111/1744-7917.12415. · DOI
  145. Sirim D, Wagner F, Wang L, Schmid RD, Pleiss J. The Laccase Engineering Database: a classification and analysis system for laccases and related multicopper oxidases. Database. 2011. https://doi.org/10.1093/database/bar006. · DOI
  146. Liu Z, Xie T, Zhong Q, Wang G. Crystal structure of CotA laccase complexed with 2, 2-azinobis-(3-ethylbenzothiazoline-6-sulfonate) at a novel binding site. Acta Crystallogr Sect F Struct Biol Commun. 2016;72:328–35. https://doi.org/10.1107/S2053230X1600426X. · DOI
  147. Messerschmidt A, Ladenstein R, Huber R, Bolognesi M, Avigliano L, Petruzzelli R, Rossi A, Finazzi-Agró A. Refined crystal structure of ascorbate oxidase at 1.9 Å resolution. J Mol Biol. 1992;224:179–205. https://doi.org/10.1016/0022-2836(92)90583-6. · DOI
  148. Messerschmidt A, Luecke H, Huber R. X-ray structures and mechanistic implications of three functional derivatives of ascorbate oxidase from zucchini: reduced, peroxide and azide forms. J Mol Biol. 1993;230:997–1014. https://doi.org/10.1006/jmbi.1993.1215. · DOI
  149. Kumar SS, Phale PS, Durani S, Wangikar PP. Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng. 2003;83:386–94. https://doi.org/10.1002/bit.10681. · DOI
  150. Mehra R, Muschiol J, Meyer AS, Kepp KP. A structural-chemical explanation of fungal laccase activity. Sci Rep. 2018;8:17285. https://doi.org/10.1038/s41598-018-35633-8. · DOI
  151. Glazunova O, Trushkin N, Moiseenko K, Filimonov I, Fedorova T. Catalytic efficiency of basidiomycete laccases: redox potential versus substrate-binding pocket structure. Catalysts. 2018;8:152. https://doi.org/10.3390/catal8040152. · DOI
  152. Pardo I, Camarero S. Laccase engineering by rational and evolutionary design. Cell Mol Life Sci. 2015;72:897–910. https://doi.org/10.1007/s00018-014-1824-8. · DOI · Paper page
  153. Sitarz AK, Mikkelsen JD, Meyer AS. Structure, functionality and tuning up of laccases for lignocellulose and other industrial applications. Crit Rev Biotechnol. 2016;36:70–86. https://doi.org/10.3109/07388551.2014.949617. · DOI · Paper page
  154. Ernst HA, Jørgensen LJ, Bukh C, Piontek K, Plattner DA, Østergaard LH, Larsen S, Bjerrum MJ. A comparative structural analysis of the surface properties of asco-laccases. PLoS ONE. 2018;13:e0206589. https://doi.org/10.1371/journal.pone.0206589. · DOI
  155. Jones SM, Solomon EI. Electron transfer and reaction mechanism of laccases. Cell Mol Life Sci. 2015;72:869–83. https://doi.org/10.1007/s00018-014-1826-6. · DOI · Paper page
  156. Azimi M, Nafissi-Varcheh N, Mogharabi M, Faramarzi MA, Aboofazeli R. Study of laccase activity and stability in the presence of ionic and non-ionic surfactants and the bioconversion of indole in laccase-TX-100 system. J Mol Catal B Enzym. 2016;126:69–75. https://doi.org/10.1016/j.molcatb.2016.02.001. · DOI
  157. Kang C, Ren D, Zhang S, Zhang X, He X, Deng Z, Huang C, Guo H. Effect of polyhydroxyl compounds on the thermal stability and structure of laccase. Pol J Environ Stud. 2019;28:3253–9. https://doi.org/10.15244/pjoes/94839. · DOI
  158. Díaz R, Díaz-Godínez G, Anducho-Reyes MA, Mercado-Flores Y, Herrera-Zúñiga LD. In silico design of laccase thermostable mutants from Lacc 6 of Pleurotus ostreatus. Front Microbiol. 2018;9:1–12. https://doi.org/10.3389/fmicb.2018.02743. · DOI
  159. Drozd R, Rakoczy R, Wasak A, Junka A, Fijałkowski K. The application of magnetically modified bacterial cellulose for immobilization of laccase. Int J Biol Macromol. 2018;108:462–70. https://doi.org/10.1016/j.ijbiomac.2017.12.031. · DOI
  160. Mateljak I, Rice A, Yang K, Tron T, Alcalde M. The generation of thermostable fungal laccase chimeras by SCHEMA-RASPP structure-guided recombination in vivo. ACS Synth Biol. 2019;8:833–43. https://doi.org/10.1021/acssynbio.8b00509. · DOI
  161. Herrera-Zúñiga LD, Millán-Pacheco C, Viniegra-González G, Villegas E, Arregui L, Rojo-Domínguez A. Molecular dynamics on laccase from Trametes versicolor to examine thermal stability induced by salt bridges. Chem Phys. 2019;517:253–64. https://doi.org/10.1016/j.chemphys.2018.10.019. · DOI
  162. Lassouane F, Aït-Amar H, Amrani S, Rodriguez-Couto S. A promising laccase immobilization approach for bisphenol A removal from aqueous solutions. Bioresour Technol. 2019;271:360–7. https://doi.org/10.1016/j.biortech.2018.09.129. · DOI · Paper page
  163. Llevot A, Grau E, Carlotti S, Grelier S, Cramail H. Selective laccase-catalyzed dimerization of phenolic compounds derived from lignin: towards original symmetrical bio-based (bis) aromatic monomers. J Mol Catal B Enzym. 2016;125:34–41. https://doi.org/10.1016/j.molcatb.2015.12.006. · DOI
  164. Polyakov K, Gavryushov S, Ivanova S, Fedorova T, Glazunova O, Popov A, Koroleva O. Structural study of the X-ray-induced enzymatic reduction of molecular oxygen to water by Steccherinum murashkinskyi laccase: insights into the reaction mechanism. Acta Crystallogr D Struct Biol. 2017;73(Pt. 5):388–401. https://doi.org/10.1107/s2059798317003667. · DOI
  165. Gabdulkhakov A, Kostareva O, Kolyadenko I, Mikhaylina A, Trubitsina L, Tishchenko S. Incorporation of copper ions into T2/T3 centers of two-domain laccases. J Mol Biol. 2018;52:23–9. https://doi.org/10.1134/S0026893318010041. · DOI
  166. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U. Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J. 2006;273:2308–26. https://doi.org/10.1111/j.1742-4658.2006.05247.x. · DOI
  167. Awasthi M, Jaiswal N, Singh S, Pandey VP, Dwivedi UN. Molecular docking and dynamics simulation analyses unraveling the differential enzymatic catalysis by plant and fungal laccases with respect to lignin biosynthesis and degradation. J Biomol Struct Dyn. 2015;33:1835–49. https://doi.org/10.1080/07391102.2014.975282. · DOI
  168. Kjaergaard CH, Jones SM, Gounel S, Mano N, Solomon EI. Two-electron reduction versus one-electron oxidation of the type 3 pair in the multicopper oxidases. J Am Chem Soc. 2015;137:8783–94. https://doi.org/10.1021/jacs.5b04136. · DOI
  169. Patel H, Gupte S, Gahlout M, Gupte A. Purification and characterization of an extracellular laccase from solid-state culture of Pleurotus ostreatus HP-1. 3 Biotech. 2014;4:77–84. https://doi.org/10.1007/s13205-013-0129-1. · DOI · Paper page
  170. Pardo I, Santiago G, Gentili P, Lucas F, Monza E, Medrano FJ, Galli C, Martínez AT, Guallar V, Camarero S. Re-designing the substrate binding pocket of laccase for enhanced oxidation of sinapic acid. Catal Sci Technol. 2016;6:3900–10. https://doi.org/10.1039/C5CY01725D. · DOI
  171. Lucas MF, Monza E, Jørgensen LJ, Ernst HA, Piontek K, Bjerrum MJ, Martinez AT, Camarero S, Guallar V. Simulating substrate recognition and oxidation in laccases: from description to design. J Chem Theory Comput. 2017;13:1462–7. https://doi.org/10.1021/acs.jctc.6b01158. · DOI
  172. Wu MH, Lee CC, Hsiao AS, Yu SM, Wang AHJ, Ho THD. Kinetic analysis and structural studies of a high-efficiency laccase from Cerrena sp. RSD 1. FEBS Open Bio. 2018;8:1230–46. https://doi.org/10.1002/2211-5463.12459. · DOI
  173. Bertrand T, Jolivalt C, Briozzo P, Caminade E, Joly N, Madzak C, Mougin C. Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry. 2002;41:7325–33. https://doi.org/10.1021/bi0201318. · DOI
  174. Pardo I, Camarero S. Exploring the oxidation of lignin-derived phenols by a library of laccase mutants. Molecules. 2015;20:15929–43. https://doi.org/10.3390/molecules200915929. · DOI
  175. Kameshwar AKS, Barber R, Qin W. 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. J Mol Graph Model. 2018;79:15–26. https://doi.org/10.1016/j.jmgm.2017.10.019. · DOI
  176. Damas JM, Batptista AM, Soares CM. The pathway for O2 diffusion inside CotA laccase and possible implications on the multicopper oxidases family. J Chem Theory Comput. 2014;10:3525–31. https://doi.org/10.1021/ct500196e. · DOI
  177. Solomon EI, Augustine AJ, Yoon J. O2 reduction to H2O by the multicopper oxidases. Dalton Trans. 2008;30:3921–32. https://doi.org/10.1039/b800799c. · DOI
  178. Petersen LC, Degn H. Steady-state kinetics of laccase from Rhus vernicifera. Biochim Biophys Acta. 1978;526:85–92. https://doi.org/10.1016/0005-2744(78)90292-9. · DOI
  179. Stines-Chaumeil C, Roussarie E, Mano N. The nature of the rate-limiting step of blue multicopper oxidases: homogeneous studies versus heterogeneous. Biochim Open. 2017;4:36–40. https://doi.org/10.1016/j.biopen.2017.01.001. · DOI
  180. Li K, Xu F, Eriksson KEL. Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol. 1999;65:2654–60. · DOI
  181. Kulys J, Krikstopaitis K, Ziemys A, Schneider P. Laccase-catalyzed oxidation of syringates in presence of albumins. J Mol Cat B Enzym. 2002;18:99–108. https://doi.org/10.1016/S1381-1177(02)00073-5. · DOI
  182. Kurniawati S, Nicell JA. A comprehensive kinetic model of laccase-catalyzed oxidation of aqueous phenol. Biotechnol Prog. 2009;25:763–73. https://doi.org/10.1002/btpr.111. · DOI
  183. Kim SJ, Joo JC, Song BK, Yoo YJ, Kim YH. Engineering a horseradish peroxidase C stable to radical attacks by mutating multiple radical coupling sites. Biotechnol Bioeng. 2015;112:668–76. https://doi.org/10.1002/bit.25483. · DOI
  184. Dordick JS. Designing enzymes for use in organic solvents. Biotechnol Prog. 1992;8:259–67. https://doi.org/10.1021/bp00016a001. · DOI
  185. Patel N, Shahane S, Shivam, Majumdar R, Mishra U. Mode of action, properties, production, and application of laccase: a review. Recent Pat Biotechnol. 2019;13:19–32. https://doi.org/10.2174/1872208312666180821161015. · DOI
  186. Fang Z, Li T, Wang Q, Zhang X, Peng H, Fang W, Hong Y, Ge H, Xiao Y. A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Appl Microbiol Biotechnol. 2011;89:1103–10. https://doi.org/10.1007/s00253-010-2934-3. · DOI
  187. Giacobelli VG, Monza E, Lucas MF, Pezzella C, Piscitelli A, Guallar V, Sannia G. Repurposing designed mutants: a valuable strategy for computer-aided laccase engineering—the case of POXA1b. Catal Sci Technol. 2017;7:515–23. https://doi.org/10.1039/c6cy032410f. · DOI
  188. Santiago G, De Salas F, Lucas MF, Monza E, Acebes S, Martinez AT, Camarero S, Guallar V. Computer-aided laccase engineering: toward biological oxidation of arylamines. ACS Catal. 2016;6:5415–23. https://doi.org/10.1021/acscatal.6b01460. · DOI
  189. Camarero S, Pardo I, Cañas AI, Molina P, Record E, Martínez AT, Martínez MJ, Alcalde M. Engineering platforms for directed evolution of Laccase from Pycnoporus cinnabarinus. Appl Environ Microbiol. 2012;78:1370–84. https://doi.org/10.1128/AEM.07530-11. · DOI
  190. Torres-Salas P, Mate D, Ghazi I, Alcalde M. Widening the pH activity profile of a fungal laccase bye directed evolution. ChemBioChem. 2013;14(8):934–7. https://doi.org/10.1002/cbic.201300102. · DOI
  191. Xu F. Effects of redox potential and hydroxide inhibition on the pH activity profile of fungal laccases. J Biol Chem. 1997;272:924–8. https://doi.org/10.1074/jbc.272.2.924. · DOI
  192. Madzak C, Mimmi M, Caminade E, Brault A, Baumberger S, Briozzo P, Mougin C, Jolivalt C. Shifting the optimal pH of activity for a laccase from the fungus Trametes versicolor by structure-based mutagenesis. Protein Eng Des Sel. 2006;19:77–84. https://doi.org/10.1093/protein/gzj004. · DOI
  193. Zumárraga M, Bulter T, Shleev S, Polaina J, Martínez-Arias A, Plou FJ, Ballesteros A, Alcalde M. In vitro evolution of a fungal laccase in high concentrations of organic cosolvents. Chem Biol. 2007;14:1052–64. https://doi.org/10.1016/j.chembiol.2007.08.010. · DOI
  194. Avelar M, Pastor N, Ramirez-Ramirez J, Ayala M. Replacement of oxidizable residues predicted by QM-MM simulation of a fungal laccase generates variants with higher operational stability. J Inorg Biochem. 2018;178:125–33. https://doi.org/10.1016/j.jinorgbio.2017.10.007. · DOI
  195. Won DW. Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol. 2009;157:174–209. https://doi.org/10.1007/s12010-008-8279-z. · DOI
  196. Rodríguez-Couto S. Fungal laccase: a versatile enzyme for biotechnological applications. In: Yadav A, Mishra S, Singh S, Gupta A, editors. Recent advancement in white biotechnology through fungi. Fungal biology. Cham: Springer; 2019. p. 429–57. · DOI
  197. Auriol M, Filali-Meknassi Y, Adams CD, Tyagi RD, Noguerol TN, Pina B. Removal of estrogenic activity of natural and synthetic hormones from a municipal wastewater: efficiency of horseradish peroxidase and laccase from Trametes versicolor. Chemosphere. 2008;70(3):445–52. · DOI
  198. Steevensz A, Al-Ansari MM, Taylor KE, Bewtra JK, Biswas N. Comparison of soybean peroxidase with laccase in the removal of phenol from synthetic and refinery wastewater samples. J Chem Technol Biotechnol. 2009;84(5):761–9. https://doi.org/10.1002/jctb.2109. · DOI
  199. Nair RR, Demarche P, Agathos SN. Formulation and characterization of an immobilized laccase biocatalyst and its application to eliminate organic micropollutants in wastewater. New Biotechnol. 2013;30(6):814–23. https://doi.org/10.1016/j.nbt.2012.12.004. · DOI
  200. Zimmermann YS, Shahgaldian P, Corvini PFX, Hommes G. Sorption-assisted surface conjugation: a way to stabilize laccase enzyme. Appl Microbiol Biotechnol. 2011;92:169–78. https://doi.org/10.1007/s00253-011-3534-6. · DOI

200 of 205 shown

Cited by

Sorted by citations

See all 515

Metadata

Authors
Arregui, L., Ayala, M., Gómez-Gil, X., Gutiérrez-Soto, G., Hernández-Luna, C. E., Herrera de los Santos, M., Levin, L., Rojo-Domínguez, A., Romero-Martínez, D., Saparrat, M. C. N., Trujillo-Roldán, M. A., & Valdez-Cruz, N. A.
ORCID
Valdez-Cruz, Norma A.
Venue
Microbial Cell Factories
Publisher
Springer Science and Business Media LLC
Published
2019-11-14
Volume
18
Issue
1
ISSN
1475-2859
DOI
10.1186/s12934-019-1248-0
PMC
PMC6854816
Cited by
515
References
3
Language
en
Licence
Funders
Programa Iberoamericano de Ciencia y Tecnología para el Desarrollo (318RT0552 - red LACASAS INMOVILIZADAS PARA LA DEGRADACIÓN DE COMPUESTOS AROMÁTICOS EN AGUAS RESIDUALES (LIDA))

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review