Abstract
Laccases produced by Leucoagaricus gongylophorus act in lignocellulose degradation and detoxification processes. Therefore, the use of L. gongylophorus laccase (Lac1Lg) was proposed in this work for degradation of anthracene and others polycyclic aromatic hydrocarbons without the use of mediators. Degradation reactions were performed in buffer aqueous solution with 10 ppm of anthracene and other PAHs, Tween-20 in 0.25% v/v and a laccase preparation of 50 U. The optimum condition (pH 6.0 and 30 °C) was determined by response surface methodology with an excellent coefficient of determination (R2) of 0.97 and an adjusted coefficient of determination (R2adj) of 0.93. In addition, the employment of the mediator ABTS decreased the anthracene biodegradation from 44 ± 1% to 30 ± 1%. This optimum pH of 6.0 suggests that the reaction occurs by a hydrogen atom transfer mechanism. Additionally, in 24 h Lac1Lg biodegraded 72 ± 1% anthracene, 40 ± 3% fluorene and 25 ± 3% phenanthrene. The yellow laccase from L. gongylophorus biodegraded anthracene and produced anthrone and anthraquinone, which are interesting compounds for industrial applications. Moreover, this enzyme also biodegraded the PAHs phenanthrene and fluorene justifying the study of Lac1Lg for bioremediation of these compounds in the environment.
Similar content being viewed by others
References
Aljawish A, Chevalot I, Jasniewski J, Paris C, Scher J, Muniglia L (2014) Laccase-catalysed oxidation of ferulic acid and ethyl ferulate in aqueous medium: a green procedure for the synthesis of new compounds. Food Chem 145:1046–1054. https://doi.org/10.1016/j.foodchem.2013.07.119
Aylward FO, Burnum-Johnson KE, Tringe SG, Teiling C, Tremmel DM, Moeller JA, Scott JJ, Barry KW, Piehowski PD, Nicora CD, Malfatti SA, Monroe ME, Purvine SO, Goodwin LA, Smith RD, Weinstock GM, Gerardo NM, Suen G, Lipton MS, Currie CR (2013) Leucoagaricus gongylophorus produces diverse enzymes for the degradation of recalcitrant plant polymers in leaf-cutter ant fungus gardens. Appl Environ Microbiol 79:3770–3778. https://doi.org/10.1128/AEM.03833-12
Aylward FO, Khadempour L, Tremmel DM, McDonald BR, Nicora CD, Wu S, Moore RJ, Orton DJ, Monroe ME, Piehowski PD, Purvine SO, Smith RD, Lipton MS, Burnum-Johnson KE, Currie CR (2015) Enrichment and broad bepresentation of plant biomass-degrading enzymes in the specialized hyphal swellings of Leucoagaricus gongylophorus, the fungal symbiont of leaf-cutter ants. PLoS One 10:e0134752. https://doi.org/10.1371/journal.pone.0134752
Bamforth SM, Singleton I (2005) Bioremediation of polycyclic aromatic hydrocarbons: current knowledge and future directions. J Chem Technol Biotechnol 80:723–736. https://doi.org/10.1002/jctb.1276
Bicalho KU (2011) Estudo fitoquímico de Virola sebifera associado ao controle de formigas cortadeiras. Dissertation, Universidade Federal de São Carlos
Brewster CS, Sharma VK, Cizmas L, McDonald TJ (2018) Occurrence, distribution and composition of aliphatic and polycyclic aromatic hydrocarbons in sediment cores from the Lower Fox River, Wisconsin, US. Environ Sci Pollut Res 25:4974–4988. https://doi.org/10.1007/s11356-017-0819-z
Bourbonnais R, Paice MG (1992) Demethylation and delignification of kraft pulp by Tramete-versicolor in the presence of 2,2′-azinobis-(3-ethylbenzthiazoline-6-sulfonate). Appl Microbiol Biotechnol 36:823–827. https://doi.org/10.1007/bf00172202
Calado V, Montgomery D (2003) Planejamento de experimentos usando o statistica. e-papers, Rio de Janeiro
Canas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694–705. https://doi.org/10.1016/j.biotechadv.2010.05.002
de la Rubia T, Linares A, Perez J, Munoz-Dorado J, Romera J, Martinez J (2002) Characterization of manganese-dependent peroxidase isoenzymes from the ligninolytic fungus Phanerochaete flavido-alba. Res Microbiol 153:547–554. https://doi.org/10.1016/S0923-2508(02)01357-8
Chang YT, Lee JF, Liu KH, Liao YF, Yang V (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
EPA (2016) Priority chemicals. https://archive.epa.gov/epawaste/hazard/wastemin/web/html/priority.html. Accessed 10 december 2017
Farnet AM, Gil G, Ruaudel F, Chevremont AC, Ferre E (2009) Polycyclic aromatic hydrocarbon transformation with laccases of a white-rot fungus isolated from a Mediterranean schlerophyllous litter. Geoderma 149:267–271. https://doi.org/10.1016/j.geoderma.2008.12.011
Filazzola MT, Sannino F, Rao MA, Gianfreda L (1999) Effect of various pollutants and soil-like constituents on laccase from Cerrena unicolor. J Environ Qual 28:1929–1938. https://doi.org/10.2134/jeq1999.00472425002800060032x
Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369. https://doi.org/10.3389/fmicb.2016.01369
Hadibarata T, Khudhair AB, Salim MR (2012) Breakdown products in the metabolic pathway of anthracene degradation by a ligninolytic fungus Polyporus sp. S133. Water Air Soil Pollut 223:2201–2208. https://doi.org/10.1007/s11270-011-1016-1
Hadibarata T, Zubir M, Rubiyatno CTZ, Yusoff ARM, Salim MR, Fulazzaky MA, Seng B, Nugroho AE (2013) Degradation and transformation of anthracene by white-rot fungus Armillaria sp. F022. Folia Microbiol 58:385–391. https://doi.org/10.1007/s12223-013-0221-2
Hammel KE, Kalyanaraman B, Kirk TK (1986) Oxidation of polycyclic aromatic-hydrocarbons and dibenzo p-dioxins by Phanerochete chrysosporium ligninase. J Biol Chem 261:6948–6952
Han MJ, Choi HT, Song HG (2004) Degradation of phenanthrene by Trametes versicolor and its laccase. J Microbiol 42:94–98
Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137
Huang WT, Tai R, Hseu RS, Huang CT (2011) Overexpression and characterization of a thermostable, pH-stable and organic solvent-tolerant Ganoderma fornicatum laccase in Pichia pastoris. Process Biochem 46:1469–1474. https://doi.org/10.1016/j.procbio.2011.03.020
Ike PTL, Moreira AC, de Almeida FG, Ferreira D, Birolli WG, Porto ALM, Souza DHF (2015) Functional characterization of a yellow laccase from Leucoagaricus gongylophorus. Springerplus 4(654):654. https://doi.org/10.1186/s40064-015-1464-y
Jeon JR, Baldrian P, Murugesan K, Chang YS (2012) Laccase-catalysed oxidations of naturally occurring phenols: from in vivo biosynthetic pathways to green synthetic applications. Microb Biotechnol 5:318–332. https://doi.org/10.1111/j.1751-7915.2011.00273.x
Jordaan J (2005) Isolation and characterization of a novel thermostable and catalytically efficient laccase from Peniophora sp. Strain UD4. Dissertation, Rhodes University
Kudanga T, Nemadziva B, Le Roes-Hill M (2017) Laccase catalysis for the synthesis of bioactive compounds. Appl Microbiol Biotechnol 101:13–33. https://doi.org/10.1007/s00253-016-7987-5
Leontievsky A, Myasoedova N, Pozdnyakova N, Golovleva L (1997) ‘Yellow’ laccase of Panus tigrinus oxidizes non-phenolic substrates without electron-transfer mediators. FEBS Lett 413:446–448. https://doi.org/10.1016/S0014-5793(97)00953-8
Li XZ, Cheng Q, Wu YC, Feng YZ, Liu WW, Lin XG (2014a) Influencing factors and product toxicity of anthracene oxidation by fungal laccase. Pedosphere 24:359–366. https://doi.org/10.1016/S1002-0160(14)60022-9
Li XZ, Wang Y, Wu SJ, Qiu L, Gu L, Li J, Zhang B, Zhong W (2014b) Peculiarities of metabolism of anthracene and pyrene by laccase-producing fungus Pycnoporus sanguineus H1. Biotechnol Appl Biochem 61:549–554. https://doi.org/10.1002/bab.1197
Licht HHD, Boomsma JJ, Tunlid A (2014) Symbiotic adaptations in the fungal cultivar of leaf-cutting ants. Nat Commun 5:5675. https://doi.org/10.1038/ncomms6675
Madhavi V, Lele SS (2009) Laccase: properties and applications. Bioresources 4:1694–1717
Marim RA, Oliveira ACC, Marquezoni RS et al (2016) Use of sugarcane molasses by Pycnoporus sanguineus for the production of laccase for dye decolorization. Genet Mol Res 15:gmr15048972. https://doi.org/10.4238/gmr15048972
Montgomery DC (1991) Diseño y análisis de experimentos. Iberoamérica, Ciudad de México
Munusamy US, Muniandy V, Abdullah S, Pandey N, A Jones EBG (2008) Biodegradation of polycyclic aromatic hydrocarbons by laccase of Pycnoporus sanguineus and toxicity evaluation of treated PAH. Biotechnol 7:669–677. https://doi.org/10.3923/biotech.2008.669.677
Myers RH, Montgomery DC, Anderson-Cook CM (2009) Response surface methodology: process and product optimization using designed experiments. John Wiley & Sons, Hoboken
Pozdnyakova NN, Turkovskaya OV, Yudina EN, Rodakiewicz-Nowak Y (2006) Yellow laccase from the fungus Pleurotus ostreatus D1: purification and characterization. Appl Biochem Microbiol 42:56–61. https://doi.org/10.1134/S000368380601008X
Prasetyo EN, Semlitsch S, Nyanhongo GS, Lemmouchi Y, Guebitz GM (2016) Laccase oxidation and removal of toxicants released during combustion processes. Chemosphere 144:652–660. https://doi.org/10.1016/j.chemosphere.2015.07.082
Riva S (2006) Laccases: blue enzymes for green chemistry. Trends Biotechnol 24:219–226. https://doi.org/10.1016/j.tibtech.2006.03.006
Sharma M, Chaurasia PK, Yadav A, Yadav RSS, Yadava S, Yadav KDS (2016) Purification and characterization of a thermally stable yellow laccase from Daedalea flavida MTCC-145 with higher catalytic performance towards selective synthesis of substituted benzaldehydes. Russ J Bioorgan Chem 42:59–68. https://doi.org/10.1134/S1068162016010143
Tien M, Kirk T (1988) Lignin peroxidase of Phanerochaete chrysosporium. In: Wood W, Kellogg S (eds) Methods in enzymologybiomass, part b, lignin, pectin, and chitin. Academic Press, San Diego
Wolfenden BS, Willson RL (1982) Radical-cations as reference chromogens in kinetic studies of ono-electron transfer reactions: pulse radiolysis studies of 2,2′-azinobis-(3-ethylbenzthiazoline-6-sulphonate). J Chem Soc Perkin 2(7):805–812. https://doi.org/10.1039/P29820000805
Xu F (1997) Effects of redox potential and hydroxide inhibition on the pH activity profile of fungal laccases. J Biol Chem 272:924–928. https://doi.org/10.1074/jbc.272.2.924
Zeng J, Zhu QH, Wu YC, Lin XG (2016) Oxidation of polycyclic aromatic hydrocarbons using Bacillus subtilis CotA with high laccase activity and copper independence. Chemosphere 148:1–7. https://doi.org/10.1016/j.chemosphere.2016.01.019
Funding
PTLI and WGB (grant no. 141656/2014-0) thank to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their scholarships, respectively. The authors also thank CNPq (grant no. 558062/2009-1) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, grant no. 2012/19934-0) for financial support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Responsible editor: Gerald Thouand
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 114 kb)
Rights and permissions
About this article
Cite this article
Ike, P.T.L., Birolli, W.G., dos Santos, D.M. et al. Biodegradation of anthracene and different PAHs by a yellow laccase from Leucoagaricus gongylophorus. Environ Sci Pollut Res 26, 8675–8684 (2019). https://doi.org/10.1007/s11356-019-04197-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-04197-z