Tatiana Alves Rigamonte Fernandes^*, Wendel Batista da Silveira, Flávia Maria Lopes Passos, Tiago Domingues Zucchi

Show more
1Embrapa Meio Ambiente, Rodovia SP 340, Jaguariúna, Brazil 2Departamento de Microbiologia, BIOAGRO, Universidade Federal de Vi?osa, Campus Universitário, Vi?osa, Brazil.
Embrapa Meio Ambiente, Rodovia SP 340, Jaguariúna, Brazil.
Show less

Abstract: Laccases are blue multicopper enzymes, capable of oxidizing diverse aromatic and non-aromatic compounds of industrial interest, concomitantly with reduction of molecular oxygen to water. Tolerance to extreme conditions, such as high temperature, salinity or extreme pH, is required for practical industrial applications. Here we focus on bacterial laccases from the phylum Actinobacteria, notably the order Actinomycetales. Currently, less than 10 enzymes have been properly characterized, all belonging to genus Streptomyces, but it is noteworthy that all of them have exhibited industrially important properties. Furthermore, studies with enzymes from this phylum revealed a novel molecular structure of laccases, providing the basis for a distinct family, the two-domain laccases. The relevant traits of actinomycetes laccases emphasize the need for more studies involving the isolation of this bacterial group from lignin-rich environmental samples, detection of their laccase activity and thereafter, characterization of the proteins and related genes. The nonhomogeneous responses of actinomycetes laccases to traditional inhibitors, substrates or metal ions have challenged the currently accepted “laccase concept”. Finally, considering that distinguishing laccase activity in vitro from other ligninolytic enzymes becomes a difficult task due to overlaps in catalytical properties of the enzymes, we proposed a simple flow chart to help experimental assays.

Keywords: Actinomycetes, Lignin Degradation, Multicopper Oxidase, Laccases

Cite this paper: Fernandes, T. , Silveira, W. , Passos, F. and Zucchi, T. (2014) Laccases from Actinobacteria—What We Have and What to Expect. Advances in Microbiology, 4, 285-296. doi: 10.4236/aim.2014.46035.

References

[1]   Claus, H. (2004) Laccases: Structure, Reactions, Distribution. Micron, 35, 93-96.
http://dx.doi.org/10.1016/j.micron.2003.10.029

[2]   Yoshida, H. (1883) Chemistry of Lacquer (Urushi) Part 1. Journal of the Chemical Society, 43, 472-486.
http://dx.doi.org/10.1039/ct8834300472

[3]   Bertrand, G. (1896) Sur la presence simultanee de la laccase et de la tyrosinase dans le suc de quelques champignons. Comptes rendus hebdomadaires des seances de l’Academie des sciences, 123, 463-465.

[4]   Givaudan, A., Effosse, A., Faure, D., Potier, P., Bouillant, M. and Bally, R. (1993) Polyphenol Oxidase from Apospirillum lipoferum Isolated from the Rhizosphere: Evidence for a Laccase in Non-Motile Strains of Azospirillum lipoferum. FEMS Microbiology Letters, 108, 205-210.
http://dx.doi.org/10.1111/j.1574-6968.1993.tb06100.x

[5]   Piscitelli, A., Pezzella, C., Giardina, P., Faraco, V. and Giovanni, S. (2010) Heterologous Laccase Production and Its Role in Industrial Applications. Bioengineered Bugs, 1, 252-262.

[6]   Bugg, T.D.H., Ahmad, M., Hardiman, E.M. and Sing, R. (2011) The Emerging Role for Bacteria in Lignin Degradation and Bio-Product Formation. Current Opinion in Biotechnology, 22, 394-400.
http://dx.doi.org/10.1016/j.copbio.2010.10.009

[7]   Strong, P.J. and Claus, H. (2011) Laccase: A Review of Its Past and Its Future in Bioremediation. Critical Reviews in Environmental Science and Technology, 41, 373-434.
http://dx.doi.org/10.1080/10643380902945706

[8]   Bourbonnais, R. and Paice, M.G. (1990) Oxidation of Non-Phenolic Substrates—An Expanded Role for Laccase in Lignin Biodegradation. FEBS Letters, 267, 99-102.
http://dx.doi.org/10.1016/0014-5793(90)80298-W

[9]   Thurston, C.F. (1994) The Structure and Function of Fungal Laccases. Microbiology, 1, 19-26.
http://dx.doi.org/10.1099/13500872-140-1-19

[10]   Gianfreda, L., Xu, F. and Bollag, J. (1999) Laccases: A Useful Group of Oxidoreductive Enzymes. Bioremediation Journal, 3, 1-26.
http://dx.doi.org/10.1080/10889869991219163

[11]   Baldrian, P. (2005) Fungal Laccases—Occurrence and Properties. FEMS Microbiology Reviews, 30, 215-242.
http://dx.doi.org/10.1111/j.1574-4976.2005.00010.x

[12]   Giardina, P., Faraco, V., Pezzella, C., Piscitelli, A., Vanhulle, S. and Sannia, G. (2010) Laccases: A Never-Ending Story. Cellular and Molecular Life Sciences, 67, 369-385.
http://dx.doi.org/10.1007/s00018-009-0169-1

[13]   Galli, C., Gentili, P. and Jolivalt, C. (2011) How Is the Reactivity of Laccase Affected by Single-Point Mutations? Engineering Laccase for Improved Activity towards Sterically Demanding Substrates. Applied Microbiology and Biotechnology, 91, 123-131.
http://dx.doi.org/10.1007/s00253-011-3240-4

[14]   Janusz, G., Kucharzyk, K.H., Pawlik, A., Staszczak, M. and Paszczynski, A.J. (2013) Fungal Laccase, Manganese Peroxidase and Lignin Peroxidase: Gene Expression and Regulation. Enzyme and Microbial Technology, 52, 1-12.
http://dx.doi.org/10.1016/j.enzmictec.2012.10.003

[15]   Claus, H. (2003) Laccases and Their Occurrence in Prokaryotes. Archives of Microbiology, 179, 145-150.

[16]   Sharma, P., Goel, R. and Capalash, N. (2006) Bacterial Laccases. World Journal of Microbiology and Biotechnology, 23, 823-832.
http://dx.doi.org/10.1007/s11274-006-9305-3

[17]   Ball, A.S., Betts, W.B. and McCarthy, A.J. (1989) Degradation of Lignin-Related Compounds by Actinomycetes. Applied and Environmental Microbiology, 55, 1642-1644.

[18]   Kirby, R. (2005) Actinomycetes and Lignin Degradation. Advances in Applied Microbiology, 58, 125-168.
http://dx.doi.org/10.1016/S0065-2164(05)58004-3

[19]   Arias, M.E., Arenas, M., Rodriguez, J., Soliveri, J., Ball, A.S. and Hernandez, M. (2003) Kraft Pulp Biobleaching and Mediated Oxidation of a Nonphenolic Substrate by Laccase from Streptomyces cyaneus CECT 3335. Applied and Environmental Microbiology, 69, 1953-1958.
http://dx.doi.org/10.1128/AEM.69.4.1953-1958.2003

[20]   Niladevi, K.N., Jacob, N. and Prema, P. (2008) Evidence for a Halotolerant-Alkaline Laccase in Streptomyces psammoticus: Purification and Characterization. Process Biochemistry, 43, 654-660.
http://dx.doi.org/10.1016/j.procbio.2008.02.002

[21]   Gunne, M. and Urlacher, V.B. (2012) Characterization of the Alkaline Laccase Ssl1 from Streptomyces sviceus with Unusual Properties Discovered by Genome Mining. PloS ONE, 7, 1-8.

[22]   Kumar, S.V., Phale, P.S., Durani, S. and Wangikar, P.P. (2003) Combined Sequence and Structure Analysis of the Fungal Laccase Family. Biotechnology and Bioengineering, 83, 386-394.
http://dx.doi.org/10.1002/bit.10681

[23]   Sakurai, T. and Kataoka, K. (2007) Basic and Applied Features of Multicopper Oxidases, CueO, Bilirubin Oxidase, and Laccase. The Chemical Record, 7, 220-229.
http://dx.doi.org/10.1002/tcr.20125

[24]   Reiss, R., Ihssen, J., Richter, M., Eichhorn, E., Schilling, B. and Thony-Meyer, L. (2013) Laccase versus Laccase-Like Multi-Copper Oxidase: A Comparative Study of Similar Enzymes with Diverse Substrate Spectra. PLoS ONE, 8, e65633.
http://dx.doi.org/10.1371/journal.pone.0065633

[25]   Whitman, W.B., Goodfellow, M., Kampfer, P., Busse, H.J., Trujillo, M.E., Ludwig, W. and Suzuki, K.I. (2012) Bergey’s Manual of Systematic Bacteriology: The Actinobacteria. Springer Publishing Company, New York.

[26]   Goodfellow, M. and Williams, S.T. (1983) Ecology of Actinomycetes. Annual Review of Microbiology, 37, 189-216.
http://dx.doi.org/10.1146/annurev.mi.37.100183.001201

[27]   Lee, J. (1997) Biological Conversion of Lignocellulosic Biomass to Ethanol. Journal of Biotechnology, 56, 1-24.
http://dx.doi.org/10.1016/S0168-1656(97)00073-4

[28]   Godden, B., Ball, A.S., Helvenstein, P., McCarthy, A.J. and Penninckx, M. (1992) Towards Elucidation of the Lignin Degradation Pathway in Actinomycetes. Microbiology, 138, 2441-2448.
http://dx.doi.org/10.1099/00221287-138-11-2441

[29]   Taylor, C.R., Hardiman, E.M., Ahmad, M., Sainsbury, P.D., Norris, P.R. and Bugg, T.D.H. (2012) Isolation of Bacterial Strains Able to Metabolize Lignin from Screening of Environmental Samples. Journal of Applied Microbiology, 113, 521-530.
http://dx.doi.org/10.1111/j.1365-2672.2012.05352.x

[30]   Berdy, J. (2005) Bioactive Microbial Metabolites. The Journal of Antibiotics, 58, 1-26.
http://dx.doi.org/10.1038/ja.2005.1

[31]   Goodfellow, M. and Fiedler, H.P. (2010) A Guide to Successful Bioprospecting: Informed by Actinobacterial Systematic. Antonie van Leeuwenhoek, 98, 119-142.
http://dx.doi.org/10.1007/s10482-010-9460-2

[32]   Prakash, D., Nawani, N., Prakash, M., Bodas, M., Mandal, A., Khetmalas, M. and Kapadnis, B. (2013) Actinomycetes: A Repertory of Green Catalysts with a Potential Revenue Resource. BioMed Research International, 2013, Article ID: 264020.
http://dx.doi.org/10.1155/2013/264020

[33]   Endo, K., Hayashi, Y., Hibi, T., Hosono, K., Beppu, T. and Ueda, K. (2003) Enzymological Characterization of EpoA, a Laccase-Like Phenol Oxidase Produced by Streptomyces griseus. The Journal of Biochemistry, 133, 671-677.
http://dx.doi.org/10.1093/jb/mvg086

[34]   Suzuki, T., Endo, K., Ito, M., Tsujibo, H., Miyamoto, K. and Inamori, Y. (2003) A Thermostable Laccase from Streptomyces lavendulae REN-7: Purification, Characterization, Nucleotide Sequence, and Expression. Bioscience Biotechnology and Biochemistry, 67, 2167-2175.
http://dx.doi.org/10.1271/bbb.67.2167

[35]   Machczynski, M.C., Vijgenboom, E., Samyn, B. and Canters, G.W. (2004) Characterization of SLAC: A Small Laccase from Streptomyces coelicolor with Unprecedented Activity. Protein Science, 13, 2388-2397.
http://dx.doi.org/10.1110/ps.04759104

[36]   Molina-Guijarro, J.M., Perez, J., Munoz-Dorado, J., Guillen, F., Moya, R., Hernandez, M. and Arias, M.E. (2009) Detoxification of Azo Dyes by a Novel pH-Versatile, Salt-Resistant Laccase from Streptomyces ipomoea. International Microbiology, 12, 13-21.

[37]   Lu, L., Zeng, G., Fan, C., Ren, X., Wang, C., Zhao, Q., Zhang, J., Chen, M., Chen, A. and Jiang, M. (2013) Characterization of a Laccase-Like Multicopper Oxidase from Newly Isolated Streptomyces sp. C1 in Agricultural Waste Compost and Enzymatic Decolorization of Azo Dyes. Biochemical Engineering Journal, 72, 70-76.
http://dx.doi.org/10.1016/j.bej.2013.01.004

[38]   Fernandes, T.A.R., Silveira, W.B., Passos, F.M.L. and Zucchi, T.D. (2013) Characterization of a Thermotolerant Laccase Produced by Streptomyces sp. SBo86. Annals of Microbiology, Published Online.
http://dx.doi.org/10.1007/s13213-013-0781-z

[39]   Dube, E., Shareck, F., Hurtubise, Y., Daneault, C. and Beauregard, M. (2008) Homologous Cloning, Expression, and Characterisation of a Laccase from Streptomyces coelicolor and Enzymatic Decolourisation of an Indigo Dye. Applied Microbiology and Biotechnology, 79, 597-603.
http://dx.doi.org/10.1007/s00253-008-1475-5

[40]   Skalova, T., Dohnalek, J., Østergaard, L.H., Østergaard, P.R., Kolenko, P., Duskova, J., Stepankova, A. and Hasek, J. (2009) The Structure of the Small Laccase from Streptomyces coelicolor Reveals a Link between Laccases and Nitrite Reductases. Journal of Molecular Biology, 385, 1165-1178.
http://dx.doi.org/10.1016/j.jmb.2008.11.024

[41]   Alexandre, G. and Zhulin, I.B. (2000) Laccases are Widespread in Bacteria. Trends in Biotechnology, 18, 41-42.
http://dx.doi.org/10.1016/j.jmb.2008.11.024

[42]   Hakulinen, N., Kiiskinen, L.L., Kruus, K., Saloheimo, M., Paananen, A., Koivula, A. and Rouvinen, J. (2002) Crystal Structure of a Laccase from Melanocarpus albomyces with an Intact Trinuclear Copper Site. Nature Structural Biology, 9, 601-605.

[43]   Valderrama, B., Oliver, P., Medrano-Soto, A. and Vazquez-Duhalt, R. (2003) Evolutionary and Structural Diversity of Fungal Laccases. Antonie van Leeuwenhoek, 84, 289-299.
http://dx.doi.org/10.1016/j.jmb.2008.11.024

[44]   Ausec, L., Zakrzewski, M., Goesmann, A., Schlüter, A. and Mandic-Mulec, I. (2011) Bioinformatic Analysis Reveals High Diversity of Bacterial Genes for Laccase-Like Enzymes. PLoS ONE, 7, e25724
http://dx.doi.org/10.1371/journal.pone.0025724

[45]   Couto, S.R. and Herrera, T. (2006) Industrial and Biotechnological Applications of Laccases: A Review. Biotechnology Advances, 24, 500-513.
http://dx.doi.org/10.1016/j.biotechadv.2006.04.003

[46]   Kunamneni, A., Plou, F.J., Ballesteros, A. and Alcalde, M. (2008) Laccases and Their Applications: A Patent Review. Recent Patents on Biotechnology, 2, 10-24.
http://dx.doi.org/10.2174/187220808783330965

[47]   Widsten, P. and Kandelbauer, A. (2008) Laccase Applications in the Forest Products Industry: A Review. Enzyme and Microbial Technology, 42, 293-307.
http://dx.doi.org/10.1016/j.enzmictec.2007.12.003

[48]   Shraddha, R.S., Sehgal, S., Kamthania, M. and Kumar, A. (2011) Laccase: Microbial Sources, Production, Purification, and Potential Biotechnological Applications. Enzyme Research, 2011, Article ID: 217861.

[49]   Orr, I.G., Hadar, Y. and Sivan, A. (2004) Colonization, Biofilm Formation and Biodegradation of Polyethylene by a Strain of Rhodococcus ruber. Applied Microbiology and Biotechnology, 65, 97-104.

[50]   Sivan, A., Szanto, M. and Pavlov, V. (2006) Biofilm Development of the Polyethylene-Degrading Bacterium Rhodococcus ruber. Applied Microbiology and Biotechnology, 72, 346-352.
http://dx.doi.org/10.1007/s00253-005-0259-4

[51]   Mor, R. and Sivan, A. (2008) Biofilm Formation and Partial Biodegradation of Polystyrene by the Actinomycete Rhodococcus ruber. Biodegradation, 19, 851-858.
http://dx.doi.org/10.1007/s10532-008-9188-0

[52]   Osma, J.F., Toca-Herrera, J.L. and Rodriguez-Couto, S. (2010) Uses of Laccases in the Food Industry. Enzyme Research, 2010, Article ID: 918761.
http://dx.doi.org/10.4061/2010/918761

[53]   Madhavi, V. and Lele, S.S. (2009) Laccase: Properties and Applications. Bioresources, 4, 1694-1717.

[54]   Haki, G.D. and Rakshit, S.K. (2003) Developments in Industrially Important Thermostable Enzymes: A Review. Bioresource Technology, 89, 17-34.
http://dx.doi.org/10.1016/S0960-8524(03)00033-6

[55]   Hilden, K., Hakala, T.K. and Lundell, T. (2009) Thermotolerant and Thermostable Laccases. Biotechnology Letters, 31, 1117-1128.
http://dx.doi.org/10.1007/s10529-009-9998-0

[56]   Miyazaki, K. (2005) A Hyperthermophilic Laccase from Thermus thermophilus HB27. Extremophiles, 9, 415-425.
http://dx.doi.org/10.1007/s00792-005-0458-z

[57]   Couto, S.R. and Toca-Herrera, J.L. (2007) Laccase Production at Reactor Scale by Filamentous Fungi. Biotechnology Advances, 25, 558-569.
http://dx.doi.org/10.1016/j.biotechadv.2007.07.002

[58]   Li, Y., Zuo, W., Li, Y. and Wang, X. (2012) Cloning of Multicopper Oxidase Gene from Ochrobactrum sp. 531 and Characterization of Its Alkaline Laccase Activity towards Phenolic Substrates. Advances in Biological Chemistry, 2, 248-255.
http://dx.doi.org/10.4236/abc.2012.23031

[59]   Niladevi, K.N. and Prema, P. (2008) Effect of Inducers and Process Parameters on Laccase Production by Streptomyces psammoticus and Its Application in Dye Decolourization. Bioresource Technology, 99, 4583-4589.
http://dx.doi.org/10.1016/j.biortech.2007.06.056

[60]   Johannes, C. and Majcherczyk, A. (2000) Laccase Activity Tests and Laccase Inhibitors. Journal of Biotechnology, 78, 193-199.
http://dx.doi.org/10.1016/S0168-1656(00)00208-X

[61]   Ruiz-Duenas, F.J. and Martinez, A.T. (2009) Microbial Degradation of Lignin: How a Bulky Recalcitrant Polymer Is Efficiently Recycled in Nature and How We Can Take Advantage of This. Microbial Biotechnology, 2, 164-177.
http://dx.doi.org/10.1111/j.1751-7915.2008.00078.x

[62]   Harkin, J.M. and Obst, J.R. (1993) Syringaldazine, an Effective Reagent for Detecting Laccase and Peroxidase in Fungi. Experientia, 29, 381-387.
http://dx.doi.org/10.1007/BF01926734

[63]   Ahmad, M., Roberts, J.N., Hardiman, E.M., Singh, R., Eltis, L.D. and Bugg, T.D.H. (2011) Identification of DypB from Rhodococcus jostii RHA1 as a Lignin Peroxidase. Biochemistry, 50, 5096-5107.
http://dx.doi.org/10.1021/bi101892z

[64]   Anderson, C.R., Johnson, H.A., Caputo, N., Davis, R.E., Torpey, J.W. and Tebo, B.M. (2009) Mn(II) Oxidation Is Catalyzed by Heme Peroxidases in “Aurantimonas manganoxydans” Strain SI85-9A1 and Erythrobacter sp. Strain SD-21. Applied and Environmental Microbiology, 75, 4130-4138.
http://dx.doi.org/10.1128/AEM.02890-08

[65]   Hullo, M.F., Moszer, I., Danchin, A. and Martin-Verstraete, I. (2001) CotA of Bacillus subtilis Is a Copper-Dependent Laccase. Journal of Bacteriology, 183, 5426-5430.
http://dx.doi.org/10.1128/JB.183.18.5426-5430.2001

[66]   Camarero, S., Sarkar, S., Ruiz-Duenas, F.J., Martinez, M.J. and Martinez, A.T. (1999) Description of a Versatile Peroxidase Involved in the Natural Degradation of Lignin That Has Both Manganese Substrate Interaction Sites Description of a Versatile Peroxidase Involved in the Natural Degradation of Lignin That Has Both Manganese Peroxidase. The Journal of Biological Chemistry, 274, 10324-10330.

[67]   Sanchez-Amat, A. and Solano, F. (1997) A Pluripotent Polyphenol Oxidase from the Melanogenic Marine Alteromonas sp. Shares Catalytic Capabilities of Tyrosinases and Laccases. Biochemical and Biophysical Research Communications, 240, 787-792.
http://dx.doi.org/10.1006/bbrc.1997.7748

[68]   Castanera, R., Perez, G., Omarini, A., Alfaro, M., Pisabarro, A.G., Faraco, V., Amore, A. and Ramirez, L. (2012) Transcriptional and Enzymatic Profiling of Pleurotus ostreatus Laccase Genes in Submerged and Solid-State Fermentation Cultures. Applied and Environmental Microbiology, 78, 4037-4045.
http://dx.doi.org/10.1128/AEM.07880-11

[69]   Kilaru, S., Hoegger, P.J. and Kües, U. (2006) The Laccase Multi-Gene Family in Coprinopsis cinerea Has Seventeen Different Members That Divide into Two Distinct Subfamilies. Current Genetics, 50, 45-60.
http://dx.doi.org/10.1007/s00294-006-0074-1

[70]   McCaig, B.C., Meagher, R.B. and Dean, J.F.D. (2005) Gene Structure and Molecular Analysis of the Laccase-Like Multicopper Oxidase (LMCO) Gene Family in Arabidopsis thaliana. Planta, 221, 619-636.
http://dx.doi.org/10.1007/s00425-004-1472-6

[71]   Luis, P., Walther, G., Kellner, H., Martin, F. and Buscot, F. (2004) Diversity of Laccase Genes from Basidiomycetes in a Forest Soil. Soil Biology and Biochemistry, 36, 1025-1036.
http://dx.doi.org/10.1016/j.soilbio.2004.02.017

[72]   Sirim, D., Wagner, F., Wang, L., Schmid, R.D. and Pleiss, J. (2011) The Laccase Engineering Database: A Classification and Analysis System for Laccases and Related Multicopper Oxidases. Database, 2011, Article ID: bar006.
http://dx.doi.org/10.1093/database/bar006

[73]   Hoegger, P.J., Kilaru, S., James, T.Y., Thacker, J.R. and Kües, U. (2006) Phylogenetic Comparison and Classification of Laccase and Related Multicopper Oxidase Protein Sequences. FEBS Journal, 273, 2308-2326.
http://dx.doi.org/10.1111/j.1742-4658.2006.05247.x

[74]   Kellner, H., Luis, P., Zimdars, B., Kiesel, B. and Buscot, F. (2008) Diversity of Bacterial Laccase-Like Multicopper Oxidase Genes in Forest and Grassland Cambisoil Soil Samples. Soil Biology & Biochemistry, 40, 638-648.
http://dx.doi.org/10.1016/j.soilbio.2007.09.013

[75]   Ausec, L., van Elsas, J.D. and Mandic-Mulec, I. (2011) Two- and Three-Domain Bacterial Laccase-Like Genes Are Present in Drained Peat Soils. Soil Biology and Biochemistry, 43, 975-983.
http://dx.doi.org/10.1016/j.soilbio.2011.01.013

[76]   Dwivedi, U.N., Singh, P., Pandey, V.P. and Kumar, A. (2011) Structure-Function Relationship among Bacterial, Fungal and Plant Laccases. Journal of Molecular Catalysis B: Enzymatic, 68, 117-128.
http://dx.doi.org/10.1016/j.molcatb.2010.11.002

[77]   Schlosser, D., Fritsche, W. and Grey, R. (1997) Patterns of Ligninolytic Enzymes in Trametes versicolor. Distribution of Extra- and Intracellular Enzyme Activities during Cultivation on Glucose, Wheat Straw and Beech Wood. Applied and Environmental Microbiology, 47, 412-418.

[78]   Diamantidis, G., Aline, E., Bally, R. and Potier, P. (2000) Purification and Characterization of the First Bacterial Laccase in the Rhizospheric Bacterium Azospirillum lipoferum. Soil, 32, 919-927.