Advertisement

Laccases for Soil Bioremediation

  • María Pilar Guauque-TorresEmail author
  • Ana Yanina Bustos
Chapter
Part of the Microorganisms for Sustainability book series (MICRO, volume 16)

Abstract

Bioremediation tool, by diminishing noxiousness or promoting pollutant mineralization to CO2 and water, is one of the most efficient, cost-effective, and eco-friendly approaches for the rehabilitation of polluted soils. Bioremediation process is mainly based on the ability of different enzymes or complex enzymes to act on various substrates. Laccases are ligninolytic enzymes, classified as benzenediol oxygen reductase (EC 1.10.3.2) and also known as multicopper oxidases. They are widely distributed in insects, plants, archaea, fungi, and bacteria. Industrially, laccases coming from fungi are the most commonly used; however, recently bacterial laccases have attracted attention because of their versatility, which includes higher thermostability, better tolerance to different concentrations of Cu2+, and higher resistance to changes regarding pH and halo and high chloride. The versatility of laccases allows its use on the soil to polymerize pollutants, and it also permits the bioaugmentation with immobilized laccases to degrade pollutants. Taking into account that laccase is one of the oldest enzymes ever described and it is relevant to the decomposition of xenobiotics, the present chapter will be dedicated to the exploration of laccase as an invaluable tool for soil bioremediation. We will review the main aspects related to the structure of laccases, substrates, and mechanisms of action. Additionally, we will also focus on two main topics: the production and the immobilization techniques to enhance the availability and stability of laccases. We highlighted some of the successful strategies employed to enhance laccase production, including the screening of new promising laccase, recombinant laccase production, as well as different immobilization strategies applied to increase the enzyme’s stability.

Keywords

Soil bioremediation Laccases Recombinant laccase production Immobilization laccase techniques 

Notes

Acknowledgments

This work was supported by Universidad Libre de Colombia, Universidad San Pablo (Tucumán Argentina), Centro de Investigación en Biofísica, Aplicada y Alimentos (CIBAAL-CONICET) and Universidad Nacional de Santiago del Estero (UNSE) (Santiago del Estero, Argentina).

The authors acknowledge Drs. Moldes-Moreira, Sanromán-Braga, and Fernández-Fernández for permission to adapt material reprinted in this chapter.

References

  1. Abatenh E, Gizaw B, Tsegaye Z, Wassie M (2017) The role of microorganisms in bioremediation – a review. Open J Env Biol 2:38–46CrossRefGoogle Scholar
  2. Abdel-Hamid AM, Solbiati JO, Cann IKO (2013) Insights into lignin degradation and its potential industrial applications. In: Advances in applied microbiology. Elsevier, San Diego, pp 1–28Google Scholar
  3. Afreen S, Shamsi TN, Baig MA et al (2017) A novel multicopper oxidase (laccase) from cyanobacteria: purification, characterization with potential in the decolorization of anthraquinonic dye. PLoS One 12:e0175144PubMedPubMedCentralCrossRefGoogle Scholar
  4. Ahn M, Dec J, Kim JE, Bollag J (2002) Treatment of 2,4-Dichlorophenol polluted soil with free and immobilized laccase. Environ Qual 31:1509–1515CrossRefGoogle Scholar
  5. Ahn M, Zimmerman AR, Martinez CE et al (2007) Characteristics of Trametes villosa laccase adsorbed on aluminum hydroxide. Enzym Microb Technol 41:141–148.  https://doi.org/10.1016/j.enzmictec.2006.12.014 CrossRefGoogle Scholar
  6. Alsoufi MA (2018) Use of immobilized laccase in bioremediation of phenolic compounds which causes environmental pollution. J Biodivers Environ Sci 12:370–377Google Scholar
  7. Antošová Z, Sychrova H, Sychrová H, Sychrova H (2016) Yeast hosts for the production of recombinant laccases: a review. Mol Biotechnol 58:93–116.  https://doi.org/10.1007/s12033-015-9910-1 CrossRefPubMedGoogle Scholar
  8. Anwar MZ, Kim DJ, Kumar A et al (2017) SnO 2 hollow nanotubes: a novel and efficient support matrix for enzyme immobilization. Sci Rep 7:1–12.  https://doi.org/10.1038/s41598-017-15550-y CrossRefGoogle Scholar
  9. Arias ME, Rodrı J, Soliveri J et al (2003) Kraft pulp biobleaching and mediated oxidation of a nonphenolic substrate by Laccase from Streptomyces cyaneus CECT 3335, vol 69, pp 1953–1958.  https://doi.org/10.1128/AEM.69.4.1953 CrossRefGoogle Scholar
  10. Ausec L, van Elsas JD, Mandic-Mulec I (2011a) Two- and three-domain bacterial laccase-like genes are present in drained peat soils. Soil Biol Biochem 43:975–983.  https://doi.org/10.1016/j.soilbio.2011.01.013 CrossRefGoogle Scholar
  11. Ausec L, Zakrzewski M, Goesmann A et al (2011b) Bioinformatic analysis reveals high diversity of bacterial genes for laccase-like enzymes. PLoS One 6:e25724.  https://doi.org/10.1371/journal.pone.0025724 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Baldantoni D, Morelli R, Bellino A et al (2017) Anthracene and benzo(a)pyrene degradation in soil is favoured by compost amendment: perspectives for a bioremediation approach. J Hazard Mater 339:395–400.  https://doi.org/10.1016/j.jhazmat.2017.06.043 CrossRefPubMedGoogle Scholar
  13. Beppu T, Endo K, Hosono K, Ueda K (2002) A novel extracytoplasmic phenol oxidase of Streptomyces: its possible involvement in the onset of morphogenesis. Microbiology 148:1767–1776.  https://doi.org/10.1099/00221287-148-6-1767 CrossRefPubMedGoogle Scholar
  14. Bollag J (1992) Decontaminating soil with enzymes. An in situ method using phenolic and anilinic compounds. Environ Sci Technol 26:1876–1881CrossRefGoogle Scholar
  15. Bornscheuer UT, Huisman GW, Kazlauskas RJ et al (2012) Engineering the third wave of biocatalysis. Nature 485:185.  https://doi.org/10.1038/nature11117 CrossRefPubMedGoogle Scholar
  16. Botterweck J, Schmidt B, Schwarzbauer J, et al (2014) Enhanced non-extractable residue formation of 14 C-metalaxyl catalyzed by an immobilized laccase. Biol Fertil Soils 1015–1024.  https://doi.org/10.1007/s00374-014-0923-x CrossRefGoogle Scholar
  17. Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102.  https://doi.org/10.1016/0014-5793(90)80298-W CrossRefPubMedGoogle Scholar
  18. Burns RG, DeForest JL, Marxsen J et al (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234.  https://doi.org/10.1016/j.soilbio.2012.11.009 CrossRefGoogle Scholar
  19. Camacho-Cordova D, Morales-Borges R (2009) Immobilization of laccase on hybrid layered double hydroxide. Quim Nova 32:1495–1499CrossRefGoogle Scholar
  20. Chandra R, Chowdhary P (2015) Properties of bacterial laccases and their application in bioremediation of industrial wastes. Environ Sci Process Impacts 17:326–342.  https://doi.org/10.1039/C4EM00627E CrossRefPubMedGoogle Scholar
  21. Chang Y-T, Lee J-F, Liu K-H et al (2016) Immobilization of fungal laccase onto a nonionic surfactant-modified clay material: application to PAH degradation. Environ Sci Pollut Res 23:4024–4035.  https://doi.org/10.1007/s11356-015-4248-6 CrossRefGoogle Scholar
  22. Chen Q, Marshall MN, Geib SM et al (2012) Effects of laccase on lignin depolymerization and enzymatic hydrolysis of ensiled corn Stover. Bioresour Technol 117:186–192.  https://doi.org/10.1016/j.biortech.2012.04.085 CrossRefPubMedGoogle Scholar
  23. Chen L, Zou M, Hong FF (2015) Evaluation of fungal laccase immobilized on natural nanostructured bacterial cellulose. Front Microbiol 6:1245.  https://doi.org/10.3389/fmicb.2015.01245 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Chirnside AEM, Ritter WF, Radosevich M (2011) Biodegradation of aged residues of atrazine and alachlor in a mix-load site soil by fungal enzymes. Appl Environ Soil Sci 2011:1–10.  https://doi.org/10.1155/2011/658569 CrossRefGoogle Scholar
  25. Compart LCA, Machado KMG, Matheus DR, Cardoso AV (2007) Immobilization of Psilocybe castanella on ceramic (slate) supports and its potential for soil bioremediation. World J Microbiol Biotechnol 23:1479–1483.  https://doi.org/10.1007/s11274-007-9393-8 CrossRefGoogle Scholar
  26. Correa S, Puertas S, Gutiérrez L et al (2019) Design of stable magnetic hybrid nanoparticles of Si-entrapped HRP. PLoS One 14:e0214004.  https://doi.org/10.1371/journal.pone.0214004 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Couto SR, Herrera JLT (2006) Industrial and biotechnological applications of laccases: a review. Biotechnol Adv 24:500–513CrossRefGoogle Scholar
  28. Couto SR, Toca-Herrera JL (2007) Laccase production at reactor scale by filamentous fungi. Biotechnol Adv 25:558–569PubMedCrossRefGoogle Scholar
  29. Dai Y, Yin L, Niu J (2011) Laccase-carrying electrospun fibrous membranes for adsorption and degradation of PAHs in shoal soils. Environ Sci Technol 45:10611–10618.  https://doi.org/10.1021/es203286e CrossRefPubMedGoogle Scholar
  30. Dayi B, Duishemambet Kyzy A, Akdogan HA (2018) Characterization of recuperating talent of white-rot fungi cells to dye-contaminated soil/water. Chin J Chem Eng 27:634.  https://doi.org/10.1016/j.cjche.2018.05.004 CrossRefGoogle Scholar
  31. De Lima DP, Dos Santos E dos A, Marques MR et al (2018) Fungal bioremediation of pollutant aromatic amines. Curr Opin Green Sustain Chem 11:34–44.  https://doi.org/10.1016/j.cogsc.2018.03.012 CrossRefGoogle Scholar
  32. Desai SS, Nityanand C (2011) Microbial laccases and their applications: a review. Asian J Biotechnol 3:98–124.  https://doi.org/10.3923/ajbkr.2011.98.124 CrossRefGoogle Scholar
  33. Dias AA, Matos AJS, Fraga I et al (2017) An easy method for screening and detection of laccase activity. Open Biotechnol J 11:89CrossRefGoogle Scholar
  34. Dodor DE, Hwang H, Ekunwe SI (2004) Oxidation of anthracene and benzo[a]pyrene by immobilized laccase from Trametes versicolor. Enzym Microb Technol 35:210–217.  https://doi.org/10.1016/j.enzmictec.2004.04.007 CrossRefGoogle Scholar
  35. Dodor DE, Miyittah M, Ahiabor BDK (2018) Immobilized laccase mediator-catalyzed oxidation of aqueous mixtures of polycyclic aromatic hydrocarbons. Polycycl Aromat Compd 0:1–11. doi:  https://doi.org/10.1080/10406638.2018.1462210
  36. Driks A (1999) Bacillus subtilis spore coat. Microbiol Mol Biol Rev 63:1–20PubMedPubMedCentralGoogle Scholar
  37. Dubé E, Shareck F, Hurtubise Y et al (2008) Homologous cloning, expression, and characterisation of a laccase from Streptomyces coelicolor and enzymatic decolourisation of an indigo dye. Appl Microbiol Biotechnol 79:597–603.  https://doi.org/10.1007/s00253-008-1475-5 CrossRefPubMedGoogle Scholar
  38. 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 28:83–99.  https://doi.org/10.1016/S0926-3373(00)00168-5 CrossRefGoogle Scholar
  39. Durao P, Chen Z, Fernandes AT et al (2008) Copper incorporation into recombinant CotA laccase from Bacillus subtilis: characterization of fully copper loaded enzymes. JBIC J Biol Inorg Chem 13:183–193PubMedCrossRefGoogle Scholar
  40. Eichlerová I, Šnajdr J, Baldrian P (2012) Laccase activity in soils: considerations for the measurement of enzyme activity. Chemosphere 88:1154–1160.  https://doi.org/10.1016/j.chemosphere.2012.03.019 CrossRefPubMedGoogle Scholar
  41. Endo K, Hayashi Y, Hibi T et al (2003) Enzymological characterization of EpoA, a laccase-like phenol oxidase produced by Streptomyces griseus. J Biochem 133:671–677PubMedCrossRefGoogle Scholar
  42. Ergün BG, Çalık P, Gündüz Ergün B, Çalık P (2016) Lignocellulose degrading extremozymes produced by Pichia pastoris: current status and future prospects. Bioprocess Biosyst Eng 39:1–36.  https://doi.org/10.1007/s00449-015-1476-6 CrossRefPubMedGoogle Scholar
  43. Fang Z, Li T, Wang Q et al (2011) A bacterial laccase from marine microbial metagenome exhibiting chloride tolerance and dye decolorization ability. Appl Microbiol Biotechnol 89:1103–1110.  https://doi.org/10.1007/s00253-010-2934-3 CrossRefPubMedGoogle Scholar
  44. Fang Z-M, Li T-L, Chang F et al (2012) A new marine bacterial laccase with chloride-enhancing, alkaline-dependent activity and dye decolorization ability. Bioresour Technol 111:36–41.  https://doi.org/10.1016/j.biortech.2012.01.172 CrossRefPubMedGoogle Scholar
  45. Fang Z, Liu X, Chen L et al (2015) Identification of a laccase Glac15 from Ganoderma lucidum 77002 and its application in bioethanol production. Biotechnol Biofuels 8:54.  https://doi.org/10.1186/s13068-015-0235-x CrossRefPubMedPubMedCentralGoogle Scholar
  46. FAO (2017) Voluntary guidelines for sustainable soil management. 155th Session of the FAO Council, Rome, Italy, 5th December 2016 15Google Scholar
  47. Fernández M, Moldes D, Sanromán MA (2013) Inmovilización de Lacasa : Métodos y potenciales aplicaciones industriales. http://www.investigo.biblioteca.uvigo.es/xmlui/handle/11093/75. Accessed 07 Aug 2019
  48. Fernández-Fernández M, Sanromán MÁ, Moldes D (2013) Recent developments and applications of immobilized laccase. Biotechnol Adv 31:1808–1825.  https://doi.org/10.1016/j.biotechadv.2012.02.013 CrossRefPubMedGoogle Scholar
  49. Ferrer-Miralles N, Domingo-Espín J, Corchero JL et al (2009) Microbial factories for recombinant pharmaceuticals. Microb Cell Factories 8:17CrossRefGoogle Scholar
  50. Food and Agricultural Organization of the United States (FAO), Intergovernmental Technical Panel on Soils (ITPS) (2015) Status of the world ’ s soil resources (SWSR) – main report. FAO, RomeGoogle Scholar
  51. Fu M, Xing J, Ge Z (2019) Preparation of laccase-loaded magnetic nanoflowers and their recycling for efficient degradation of bisphenol A. Sci Total Environ 651:2857–2865.  https://doi.org/10.1016/j.scitotenv.2018.10.145 CrossRefPubMedGoogle Scholar
  52. García-Rivero M, Peralta-Perez M (2008) Cometabolismo en la biodegradación de hidrocarburos cometabolism in the biodegradation of hydrocarbons. Rev Mex Ing Quim 7:1–12Google Scholar
  53. Gianfreda L, Bollag J-MJ-M (1994) Effect of soils on the behavior of immobilized enzymes. Soil Sci Soc Am J 58:1672–1681.  https://doi.org/10.2136/sssaj1994.03615995005800060014x CrossRefGoogle Scholar
  54. 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 108:205–210.  https://doi.org/10.1111/j.1574-6968.1993.tb06100.x CrossRefGoogle Scholar
  55. Gu C, Zheng F, Long L et al (2014) Engineering the expression and characterization of two novel laccase isoenzymes from Coprinus comatus in Pichia pastoris by fusing an additional ten amino acids tag at N-terminus. PLoS One 9:e93912.  https://doi.org/10.1371/journal.pone.0093912 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Guan Z-B, Zhang N, Song C-M et al (2014) Molecular cloning, characterization, and dye-decolorizing ability of a temperature-and pH-stable laccase from Bacillus subtilis X1. Appl Biochem Biotechnol 172:1147–1157PubMedCrossRefGoogle Scholar
  57. Guan ZB, Luo Q, Wang HR et al (2018) Bacterial laccases: promising biological green tools for industrial applications. Cell Mol Life Sci 75:3569–3592.  https://doi.org/10.1007/s00018-018-2883-z CrossRefPubMedGoogle Scholar
  58. Guauque-Torres M, Foresti M, Ferreira M (2013) Cross-linked enzyme aggregates (CLEAs) of selected lipases: a procedure for the proper calculation of their recovered activity. AMB Express 3:25.  https://doi.org/10.1186/2191-0855-3-25 CrossRefPubMedCentralPubMedGoogle Scholar
  59. Guebitz G, Cavaco PA, Kandelbauer A, et al (2003) Biocatalyst containing a laccase. Patent EP1468968 (A1)Google Scholar
  60. Gupta N, Farinas ET (2010) Directed evolution of CotA laccase for increased substrate specificity using Bacillus subtilis spores. Protein Eng Des Sel 23:679–682.  https://doi.org/10.1093/protein/gzq036 CrossRefPubMedGoogle Scholar
  61. Hatamoto O, Sekine H, Nakano E, ABE K (1999) Cloning and expression of a cDNA encoding the laccase from Schizophyllum commune. Biosci Biotechnol Biochem 63:58–64PubMedCrossRefGoogle Scholar
  62. Ihssen J, Reiss R, Luchsinger R et al (2015) Biochemical properties and yields of diverse bacterial laccase-like multicopper oxidases expressed in Escherichia coli. Sci Rep 5:10465.  https://doi.org/10.1038/srep10465 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Iimura Y, Katayama Y, Kawai S et al (1995) Degradation and Solubilization of 13 C_, 14 C-side chain labeled synthetic lignin (Dehydrogenative Polymerizate) by laccase III of Coriolus versicolor. Biosci Biotechnol Biochem 59:903–905.  https://doi.org/10.1271/bbb.59.903 CrossRefGoogle Scholar
  64. Iimura Y, Sonoki T, Habe H (2018) Heterologous expression of Trametes versicolor laccase in Saccharomyces cerevisiae. Protein Expr Purif 141:39–43.  https://doi.org/10.1016/j.pep.2017.09.004 CrossRefPubMedGoogle Scholar
  65. Iracheta-Cárdenas MM, Rocha-Peña MA, Galán-Wong LJ et al (2016) A Pycnoporus sanguineus laccase for denim bleaching and its comparison with an enzymatic commercial formulation. J Environ Manag 177:93–100.  https://doi.org/10.1016/j.jenvman.2016.04.008 CrossRefGoogle Scholar
  66. Iyer HV, Przybycien TM (1995) Metal affinity protein precipitation: effects of mixing, protein concentration, and modifiers on protein fractionation. Biotechnol Bioeng 48:324–332.  https://doi.org/10.1002/bit.260480405 CrossRefPubMedGoogle Scholar
  67. Kajita S, Sugawara S, Miyazaki Y et al (2004) Overproduction of recombinant laccase using a homologous expression system in Coriolus versicolor. Appl Microbiol Biotechnol 66:194–199.  https://doi.org/10.1007/s00253-004-1663-x CrossRefPubMedGoogle Scholar
  68. 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 7:707.  https://doi.org/10.3389/fmicb.2016.00707 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Kiiskinen L-L (2004) Expression of Melanocarpus albomyces laccase in Trichoderma reesei and characterization of the purified enzyme. Microbiology 150:3065–3074.  https://doi.org/10.1099/mic.0.27147-0 CrossRefPubMedGoogle Scholar
  70. Kim C, Lorenz WW, Hoopes JT, Dean JFD (2001) Oxidation of phenolate siderophores by the multicopper oxidase encoded by the Escherichia coli yacK gene. J Bacteriol 183:4866–4875PubMedPubMedCentralCrossRefGoogle Scholar
  71. Koschorreck K, Richter SM, Ene AB et al (2008) Cloning and characterization of a new laccase from Bacillus licheniformis catalyzing dimerization of phenolic acids. Appl Microbiol Biotechnol 79:217–224PubMedCrossRefGoogle Scholar
  72. Koschorreck K, Schmid RD, Urlacher VB (2009) Improving the functional expression of a Bacillus licheniformis laccase by random and site-directed mutagenesis. BMC Biotechnol 9:12.  https://doi.org/10.1186/1472-6750-9-12 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Košnář Z, Částková T, Wiesnerová L et al (2018) Comparing the removal of polycyclic aromatic hydrocarbons in soil after different bioremediation approaches in relation to the extracellular enzyme activities. J Environ Sci (China) 76:1–10.  https://doi.org/10.1016/j.jes.2018.05.007 CrossRefGoogle Scholar
  74. Koyani RD, Vazquez-Duhalt R (2016) Laccase encapsulation in chitosan nanoparticles enhances the protein stability against microbial degradation. Environ Sci Pollut Res 23:18850–18857.  https://doi.org/10.1007/s11356-016-7072-8 CrossRefGoogle Scholar
  75. Kumar A, Kanwar SS (2012) An innovative approach to immobilize lipase onto natural fiber and its application for the synthesis of 2-Octyl Ferulate in an organic medium. Curr Biotechnol e 1:241–248.  https://doi.org/10.2174/2211550111201030241 CrossRefGoogle Scholar
  76. Kumar R, Kumar A, Kanwar S (2014) Synthesis of methyl succinate by natural-fibre immobilized lipase of Streptomyces sp. STL-D8. Curr Biotechnol 3:152–156.  https://doi.org/10.2174/2211550102666140107232547 CrossRefGoogle Scholar
  77. Kumar A, Kim IW, Patel SKS, Lee JK (2018) Synthesis of Protein-Inorganic Nanohybrids with Improved Catalytic Properties Using Co 3 (PO 4 ) 2. Indian J Microbiol 58:100–104.  https://doi.org/10.1007/s12088-017-0700-2 CrossRefPubMedGoogle Scholar
  78. Kumar A, Park GD, Patel SKS et al (2019) SiO2 microparticles with carbon nanotube-derived mesopores as an efficient support for enzyme immobilization. Chem Eng J 359:1252–1264.  https://doi.org/10.1016/j.cej.2018.11.052 CrossRefGoogle Scholar
  79. Lawton TJ, Rosenzweig AC (2011) Detection and characterization of a multicopper oxidase from nitrosomonas Europaea, 1st edn. Elsevier Inc, AmsterdamGoogle Scholar
  80. Lee HR, Chung M, Kim MI, Ha SH (2017) Preparation of glutaraldehyde-treated lipase-inorganic hybrid nanoflowers and their catalytic performance as immobilized enzymes. Enzym Microb Technol 105:24–29.  https://doi.org/10.1016/J.ENZMICTEC.2017.06.006 CrossRefGoogle Scholar
  81. Lettera V, Pezzella C, Cicatiello P et al (2016) Efficient immobilization of a fungal laccase and its exploitation in fruit juice clarification. Food Chem 196:1272–1278.  https://doi.org/10.1016/j.foodchem.2015.10.074 CrossRefPubMedGoogle Scholar
  82. Lisov AV, Trubitsina LI, Lisova ZA et al (2018) Transformation of humic acids by two-domain laccase from Streptomyces anulatus. Process Biochem 76:128.  https://doi.org/10.1016/j.procbio.2018.11.001 CrossRefGoogle Scholar
  83. Llorens-Blanch G, Parladé E, Martinez-Alonso M et al (2018) A comparison between biostimulation and bioaugmentation in a solid treatment of anaerobic sludge: drug content and microbial evaluation. Waste Manag 72:206–217.  https://doi.org/10.1016/J.WASMAN.2017.10.048 CrossRefPubMedGoogle Scholar
  84. Luthy RG, Ghoshal S, Ramaswami A, Nakles DV (1995) Bioslurry treatment of NAPL-contaminated soil. In: Soil and groundwater pollution. Springer, Dordrecht, pp 36–40CrossRefGoogle Scholar
  85. Ma X, Liu L, Li Q et al (2017) 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. Enzym Microb Technol 103:34–41.  https://doi.org/10.1016/j.enzmictec.2017.04.004 CrossRefGoogle Scholar
  86. Machczynski MC, Vijgenboom E, Samyn B, Canters GW (2004) Characterization of SLAC: a small laccase from Streptomyces coelicolor with unprecedented activity. Protein Sci 13:2388–2397PubMedPubMedCentralCrossRefGoogle Scholar
  87. Madhavi V, Lele SS (2009) Laccase: properties and applications. BioResources 4:1694–1717.  https://doi.org/10.15376/biores.4.4.1694-1717
  88. Majeau J-A, Brar SK, Tyagi RD (2010) Laccases for removal of recalcitrant and emerging pollutants. Bioresour Technol 101:2331–2350PubMedCrossRefGoogle Scholar
  89. Majorek KA, Porebski PJ, Dayal A, Zimmerman MD, Jablonska K, Stewart AJ, Chruszcz M, Minor W (2012) Structural and immunologic characterization of bovine, horse, and rabbit serum albumins. Mol Immunol 52(3–4):174–182PubMedPubMedCentralCrossRefGoogle Scholar
  90. Martínez-Morales F, Bertrand B, Pasión Nava AA et al (2015) Production, purification and biochemical characterization of two laccase isoforms produced by Trametes versicolor grown on oak sawdust. Biotechnol Lett 37:391–396.  https://doi.org/10.1007/s10529-014-1679-y CrossRefPubMedGoogle Scholar
  91. Martins LO, Soares CM, Pereira MM et al (2002) Molecular and biochemical characterization of a highly stable bacterial laccase that occurs as a structural component of the Bacillus subtilis endospore coat. J Biol Chem 277:18849–18859PubMedCrossRefGoogle Scholar
  92. Martins LO, Durão P, Brissos V, Lindley PF (2015) Laccases of prokaryotic origin: enzymes at the interface of protein science and protein technology. Cell Mol Life Sci 72:911–922.  https://doi.org/10.1007/s00018-014-1822-x CrossRefPubMedGoogle Scholar
  93. Mate DM, Alcalde M (2015) Laccase engineering: from rational design to directed evolution. Biotechnol Adv 33:25–40PubMedCrossRefGoogle Scholar
  94. Megharaj M, Naidu R (2017) Soil and brownfield bioremediation. Microb Biotechnol 10:1244–1249.  https://doi.org/10.1111/1751-7915.12840 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Miyazaki K (2005) A hyperthermophilic laccase from Thermus thermophilus HB27. Extremophiles 9:415–425.  https://doi.org/10.1007/s00792-005-0458-z CrossRefPubMedGoogle Scholar
  96. Mohamad NR, Marzuki NHC, Buang NA et al (2015) An overview of technologies for immobilization of enzymes and surface analysis techniques for immobilized enzymes. Biotechnol Biotechnol Equip 29:205–220.  https://doi.org/10.1080/13102818.2015.1008192 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Molina-Guijarro JM, Pérez J, Muñoz-Dorado J et al (2009) Detoxification of azo dyes by a novel pH-versatile, salt-resistant laccase from Streptomyces ipomoea. Int Microbiol 12:13–21PubMedGoogle Scholar
  98. Morozova OV, Shumakovich GP, Shleev SV, Yaropolov YI (2007) Laccase-mediator systems and their applications: a review. Appl Biochem Microbiol 43:523–535.  https://doi.org/10.1134/S0003683807050055 CrossRefGoogle Scholar
  99. Mougin C, Boukcim H, Jolivat C (2009) Soil bioremediation strategies based on the use of fungal enzymes. In: Singh A, Kuhad RC, Ward OP (eds) Advances in applied bioremediation. Springer, Berlin/Heidelberg, pp 123–150CrossRefGoogle Scholar
  100. Naghdi M, Taheran M, Brar SK et al (2018) Pinewood nanobiochar: a unique carrier for the immobilization of crude laccase by covalent bonding. Int J Biol Macromol 115:563–571.  https://doi.org/10.1016/J.IJBIOMAC.2018.04.105 CrossRefPubMedGoogle Scholar
  101. Naidja A, Huang PM, Bollag J-M (2000) Enzyme-clay interactions and their impact on transformations of natural and anthropogenic organic compounds in soil. J Environ Qual 29:677.  https://doi.org/10.2134/jeq2000.00472425002900030002x CrossRefGoogle Scholar
  102. Neifar M, Chouchane H, Mahjoubi M et al (2016) Pseudomonas extremorientalis BU118: a new salt-tolerant laccase-secreting bacterium with biotechnological potential in textile azo dye decolourization. 3 Biotech 6:1–9.  https://doi.org/10.1007/s13205-016-0425-7 CrossRefGoogle Scholar
  103. Nikolopoulou M, Kalogerakis N (2016) Ex situ bioremediation treatment (Landfarming). In: Hydrocarbon and lipid microbiology protocols. Springer protocols handbooks. Springer, Berlin/Heidelberg, pp 195–220CrossRefGoogle Scholar
  104. Niladevi KN, Sukumaran RK, Jacob N et al (2009) Optimization of laccase production from a novel strain—Streptomyces psammoticus using response surface methodology. Microbiol Res 164:105–113.  https://doi.org/10.1016/j.micres.2006.10.006 CrossRefPubMedGoogle Scholar
  105. Nishibori N, Masaki K, Tsuchioka H et al (2013) Comparison of laccase production levels in Pichia pastoris and Cryptococcus sp. S-2. J Biosci Bioeng 115:394–399.  https://doi.org/10.1016/j.jbiosc.2012.10.025 CrossRefPubMedGoogle Scholar
  106. Nunes CS, Kunamneni A (2018) Laccases—properties and applications. In: Enzymes in human and animal nutrition. Elsevier, Amsterdam, pp 133–161CrossRefGoogle Scholar
  107. Olajuyigbe FM, Fatokun CO (2017) Biochemical characterization of an extremely stable pH-versatile laccase from Sporothrix carnis CPF-05. Int J Biol Macromol 94:535–543PubMedCrossRefGoogle Scholar
  108. Osma JF, Toca-Herrera JL, Rodríguez-Couto S (2010) Uses of laccases in the food industry. Enzyme Res 2010:1–8.  https://doi.org/10.4061/2010/918761 CrossRefGoogle Scholar
  109. Outten FW, Huffman DL, Hale JA, O’Halloran TV (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276:30670–30677PubMedCrossRefGoogle Scholar
  110. Pant A, Rai JPN (2018) Bioremediation of chlorpyrifos contaminated soil by two phase bioslurry reactor: processes evaluation and optimization by Taguchi’s design of experimental (DOE) methodology. Ecotoxicol Environ Saf 150:305–311.  https://doi.org/10.1016/J.ECOENV.2017.12.052 CrossRefPubMedGoogle Scholar
  111. Pardo I, Camarero S (2015) Laccase engineering by rational and evolutionary design. Cell Mol Life Sci 72:897–910PubMedPubMedCentralCrossRefGoogle Scholar
  112. Piontek K, Antorini M, Choinowski T (2002) Crystal structure of a laccase from the fungus Trametes versicolor at 1.90-?? Resolution containing a full complement of coppers. J Biol Chem 277:37663–37669.  https://doi.org/10.1074/jbc.M204571200 CrossRefPubMedGoogle Scholar
  113. Piscitelli A, Pezzella C, Giardina P et al (2010) Heterologous laccase production and its role in industrial applications. Bioeng Bugs 1:254–264.  https://doi.org/10.4161/bbug.1.4.11438 CrossRefGoogle Scholar
  114. Quintero Díaz JC (2011) Revisión: degradación de plaguicidas mediante hongos de la pudrición blanca de la madera. Rev Fac Nac Agron Medellín 64:5867–5882Google Scholar
  115. Record E, Punt PJ, Chamkha M et al (2002) Expression of the Pycnoporus cinnabarinus laccase gene in Aspergillus Niger and characterization of the recombinant enzyme. Eur J Biochem 269:602–609PubMedCrossRefGoogle Scholar
  116. Reiss R, Ihssen J, Thöny-Meyer L (2011) Bacillus pumilus laccase: a heat stable enzyme with a wide substrate spectrum. BMC Biotechnol 11:9PubMedPubMedCentralCrossRefGoogle Scholar
  117. Rezaei S, Shahverdi AR, Faramarzi MA (2017) Isolation, one-step affinity purification, and characterization of a polyextremotolerant laccase from the halophilic bacterium Aquisalibacillus elongatus and its application in the delignification of sugar beet pulp. Bioresour Technol 230:67–75PubMedCrossRefGoogle Scholar
  118. Román R, Torres-Duarte C, Ayala M, Vázquez-Duhalt R (2010) Producción a escala piloto de lacasa de Coriolopsis gallica. Rev Mex Micol 32:1.2Google Scholar
  119. Rosano GL, Ceccarelli EA (2014) Recombinant protein expression in Escherichia coli: advances and challenges. Front Microbiol 5:172.  https://doi.org/10.3389/fmicb.2014.00172 CrossRefPubMedPubMedCentralGoogle Scholar
  120. Ruggiero P, Sarkar J, Bollag J (1989) Detoxification of 2,4 dichlorophenol by a laccase immobilized on soil or clay. Soil Sci Soc Am J 147:361–370CrossRefGoogle Scholar
  121. Saloheimo M, Niku-Paavola M-L (1991) Heterologous production of a Ligninolytic enzyme: expression of the Phlebia Radiata laccase gene in Trichoderma Reesei. Bio/Technology 9:987–990.  https://doi.org/10.1038/nbt1091-987 CrossRefGoogle Scholar
  122. Saptarshi SR, Duschl A, Lopata AL (2013) Interaction of nanoparticles with proteins: relation to bio-reactivity of the nanoparticle. J Nanobiotechnology 11:26.  https://doi.org/10.1186/1477-3155-11-26 CrossRefPubMedPubMedCentralGoogle Scholar
  123. Šašek V, Glaser JA, Baveye P (2003) The utilization of bioremediation to reduce soil contamination: problems and solutions. Springer, DordrechtCrossRefGoogle Scholar
  124. Shannon MJR, Bartha R (1988) Immobilization of leachable toxic soil pollutants by using oxidative enzymes. Appl Environ Microbiol 54:1719–1723PubMedPubMedCentralGoogle Scholar
  125. Shiomi N (2015) Advances in bioremediation of wastewater and polluted soil. AvE4EvAGoogle Scholar
  126. Shraddha SR, Sehgal S et al (2011) Laccase: microbial sources, production, purification, and potential biotechnological applications. Enzyme Res 2011:217861.  https://doi.org/10.4061/2011/217861 CrossRefPubMedPubMedCentralGoogle Scholar
  127. Si J, Peng F, Cui B (2013) Purification, biochemical characterization and dye decolorization capacity of an alkali-resistant and metal-tolerant laccase from Trametes pubescens. Bioresour Technol 128:49–57.  https://doi.org/10.1016/j.biortech.2012.10.085 CrossRefPubMedGoogle Scholar
  128. Singh G, Bhalla A, Kaur P et al (2011) Laccase from prokaryotes: a new source for an old enzyme. Rev Environ Sci Bio/Technol 10:309–326.  https://doi.org/10.1007/s11157-011-9257-4 CrossRefGoogle Scholar
  129. Siracusa G, Becarelli S, Lorenzi R et al (2017) PCB in the environment: bio-based processes for soil decontamination and management of waste from the industrial production of Pleurotus ostreatus. New Biotechnol 39:232–239.  https://doi.org/10.1016/J.NBT.2017.08.011 CrossRefGoogle Scholar
  130. Song JE, Su J, Noro J et al (2018) Bio-coloration of bacterial cellulose assisted by immobilized laccase. AMB Express:8.  https://doi.org/10.1186/s13568-018-0552-0
  131. Sonoki T, Kajita S, Ikeda S et al (2005) Transgenic tobacco expressing fungal laccase promotes the detoxification of environmental pollutants. Appl Microbiol Biotechnol 67:138–142.  https://doi.org/10.1007/s00253-004-1770-8 CrossRefPubMedGoogle Scholar
  132. Speight JG, El-Gendy NS (2018) Bioremediation of contaminated soil. In: Introduction to petroleum biotechnology. Elsevier, Amsterdam, pp 361–417CrossRefGoogle Scholar
  133. Su J, Noro J, Fu J et al (2018) Exploring PEGylated and immobilized laccases for catechol polymerization. AMB Express 8.  https://doi.org/10.1186/s13568-018-0665-5
  134. Surridge AKJ, Wehner FC, Cloete TE (2009) Bioremediation of polluted soil. In: Singh A, Kuhad RC, Ward OP (eds) Advances in applied bioremediation. Springer, Berlin/HeidelbergGoogle Scholar
  135. Suzuki T, Endo K, Ito M et al (2003) A thermostable laccase from Streptomyces lavendulae REN-7: purification, characterization, nucleotide sequence, and expression. Biosci Biotechnol Biochem 67:2167–2175PubMedCrossRefGoogle Scholar
  136. 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. Enzym Microb Technol 38:665–669CrossRefGoogle Scholar
  137. Theuerl S, Buscot F (2010) Laccases: toward disentangling their diversity and functions in relation to soil organic matter cycling. Biol Fertil Soils 46:215–225.  https://doi.org/10.1007/s00374-010-0440-5 CrossRefGoogle Scholar
  138. Upadhyay P, Shrivastava R, Agrawal PK (2016) Bioprospecting and biotechnological applications of fungal laccase. 3. Biotech 6:15.  https://doi.org/10.1007/s13205-015-0316-3 CrossRefGoogle Scholar
  139. Van De Vijver E, Van Meirvenne M, Seuntjens P (2015) Investigating bioremediation of petroleum hydrocarbons through landfarming using apparent electrical conductivity measurements. EGU Gen Assem 2015, held 12-17 April 2015 Vienna, Austria id9304 17Google Scholar
  140. Verma R, Kumar A, Kumar S (2019) Synthesis and characterization of cross-linked enzyme aggregates (CLEAs) of thermostable xylanase from Geobacillus thermodenitrificans X1. Process Biochem 80:72–79.  https://doi.org/10.1016/j.procbio.2019.01.019 CrossRefGoogle Scholar
  141. Viswanath B, Rajesh B, Janardhan A et al (2014) Fungal laccases and their applications in bioremediation. Enzyme Res 2014:1–21.  https://doi.org/10.1155/2014/163242 CrossRefGoogle Scholar
  142. Wang T-N, Lu L, Wang J-Y, Xu T-F, Li J, Zhao M (2015) Enhanced expression of an industry applicable CotA laccase from Bacillus subtilis in Pichia pastoris by non-repressing carbon sources together with pH adjustment: recombinant enzyme characterization and dye decolorization. Process Biochem 50(1):97–103CrossRefGoogle Scholar
  143. Wang X, Yao M, Liu L et al (2016) Degradation of chlorpyrifos in contaminated soil by immobilized laccase. J Serbian Chem Soc 81:1215–1224.  https://doi.org/10.2298/JSC160128066W CrossRefGoogle Scholar
  144. Wang J, Lu L, Feng F (2017a) Combined strategies for improving production of a thermo-alkali stable laccase in Pichia pastoris. Electron J Biotechnol 28:7–13.  https://doi.org/10.1016/j.ejbt.2017.04.002 CrossRefGoogle Scholar
  145. Wang X, Liu L, Yao M, et al (2017b) Degradation of carbofuran in contaminated soil by immobilized laccase. Polish J Environ Stud 26:1305–1312.  https://doi.org/10.15244/pjoes/68428 CrossRefGoogle Scholar
  146. Wang X, Shi Y, Ni Z et al (2018) Degradation of polycyclic aromatic hydrocarbons in contaminated soil by immobilized laccase. J Serbian Chem Soc 83:549–559.  https://doi.org/10.2298/JSC171004022W CrossRefGoogle Scholar
  147. Wen X, Du C, Wan J et al (2019) Immobilizing laccase on kaolinite and its application in treatment of malachite green effluent with the coexistence of cd (П). Chemosphere 217:843–850.  https://doi.org/10.1016/j.chemosphere.2018.11.073 CrossRefPubMedGoogle Scholar
  148. Wu Y, Jiang Y, Jiao J et al (2014) Adsorption of Trametes versicolor laccase to soil iron and aluminum minerals: enzyme activity, kinetics and stability studies. Colloids Surf B Biointerf 114:342–348.  https://doi.org/10.1016/j.colsurfb.2013.10.016 CrossRefGoogle Scholar
  149. Xie H, Liu H, Xie Y et al (2015) Fabrication of a novel immobilization system and its application for removal of anthracene from soil. Biochem Eng J 97:8–16.  https://doi.org/10.1016/j.bej.2015.01.011 CrossRefGoogle Scholar
  150. Yang J, Ng TB, Lin J, Ye X (2015) A novel laccase from basidiomycete Cerrena sp.: cloning, heterologous expression, and characterization. Int J Biol Macromol 77:344–349PubMedCrossRefGoogle Scholar
  151. Yang J, Lin Q, Ng TB, Ye X, Lin J, Rito-Palomares M (2014) Purification and characterization of a novel Laccase from Cerrena sp. HYB07 with dye decolorizing ability. PLoS One 9(10):e110834PubMedPubMedCentralCrossRefGoogle Scholar
  152. Yang J, Wang G, Ng TB, et al (2016a) Laccase production and differential transcription of laccase genes in Cerrena sp. in response to metal ions, aromatic compounds, and nutrients. Front Microbiol 6:1558Google Scholar
  153. Yang J, Xu X, Ng TB et al (2016b) Laccase gene family in Cerrena sp. HYB07: sequences, heterologous expression and transcriptional analysis. Molecules 21:1017PubMedCentralCrossRefPubMedGoogle Scholar
  154. Yang J, Xu X, Yang X et al (2016c) Cross-linked enzyme aggregates of Cerrena laccase: preparation, enhanced NaCl tolerance and decolorization of Remazol brilliant blue reactive. J Taiwan Inst Chem Eng 65:1–7.  https://doi.org/10.1016/J.JTICE.2016.04.025 CrossRefGoogle Scholar
  155. Yang J, Li W, Bun Ng T et al (2017) Laccases: production, expression regulation, and applications in pharmaceutical biodegradation. Front Microbiol 8:832.  https://doi.org/10.3389/fmicb.2017.00832 CrossRefPubMedPubMedCentralGoogle Scholar
  156. Yoshida H (1883) LXIII.—chemistry of lacquer (Urushi). Part I. communication from the chemical society of Tokyo. J Chem Soc Trans 43:472–486CrossRefGoogle Scholar
  157. Yoshitake A, Katayama Y, Nakamura M et al (1993) N-linked carbohydrate chains protect laccase III from proteolysis in Coriolus versicolor. J Gen Microbiol 139:179–185.  https://doi.org/10.1099/00221287-139-1-179 CrossRefGoogle Scholar
  158. Zdarta J, Meyer AS, Jesionowski T, Pinelo M (2018) Developments in support materials for immobilization of oxidoreductases: a comprehensive review. Adv Colloid Interf Sci 258:1–20.  https://doi.org/10.1016/j.cis.2018.07.004 CrossRefGoogle Scholar
  159. Zeng J, Lin X, Zhang J et al (2011) Oxidation of polycyclic aromatic hydrocarbons by the bacterial laccase CueO from E. coli. Appl Microbiol Biotechnol 89:1841–1849PubMedCrossRefGoogle Scholar
  160. Zhang Y, Dong X, Jiang Z et al (2013) Assessment of the ecological security of immobilized enzyme remediation process with biological indicators of soil health. Environ Sci Pollut Res 20:5773–5780.  https://doi.org/10.1007/s11356-012-1455-2 CrossRefGoogle Scholar
  161. Zhao Y, Ma W (2011) Method for repairing soil with DDT (Dichloro-diphenyl-Trichloroethane) pollution by fungus and enzyme combination. Patent CN102091717AGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • María Pilar Guauque-Torres
    • 1
    Email author
  • Ana Yanina Bustos
    • 2
    • 3
    • 4
  1. 1.GIAM-Z Research Group, Faculty of Environmental EngineeringUniversidad LibreSocorroColombia
  2. 2.Universidad San Pablo – TucumánSan Miguel de TucumánArgentina
  3. 3.Centro de Investigación en Biofísica, Aplicada y Alimentos (CIBAAL-CONICET)Santiago del EsteroArgentina
  4. 4.Facultad de Agronomía y Agroindustrias (FAyA)Universidad Nacional de Santiago del Estero (UNSE)Santiago del EsteroArgentina

Personalised recommendations