Evolutionary and structural diversity of fungal laccases

Abstract

Fungal laccases have been extensively exploited for industrial purposes and there is a wealth of information available regarding their reaction mechanism, biological role and several molecular aspects, including cloning, heterologous expression and transcriptional analyses. Here we present the reconstruction of the fungal laccase loci evolution inferred from the comparative analysis of 48 different sequences. The topology of the phylogenetic trees indicate that a single monophyletic branch exists for fungal laccases and that laccase isozyme genes may have evolved independently, possibly through duplication-divergence events. Laccases are copper-containing enzymes generally identified by the utilization of substituted p-diphenol substrates. Interestingly, our approach permitted the assignment of two copper-containing oxidases, preliminarily catalogued as laccases, to a different evolutionary group, distantly related to the main branch of bona fide laccases.

This is a preview of subscription content, access via your institution.

References

  1. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W. and Lipman D.J.1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res.25: 3389–3402.

    PubMed  CAS  Article  Google Scholar 

  2. Aramayo R. and Timberlake W.E.1990. Sequence and molecular structure of the Aspergillus nidulans yA (laccase I) gene. Nucl. Acids Res.18: 3415

    PubMed  CAS  Google Scholar 

  3. Berka R.M., Schneider P., Golightly E.J., Brown S., Madden M., Brown K.M., Halkier T., Mondorf K. and Xu F.1997. Characterization of the gene encoding an extracellular laccase of Myceliophthora thermophila and analysis of the recombinant enzyme expressed in Aspergillus oryzae. Appl. Environ. Microbiol.63: 3151–3157.

    PubMed  CAS  Google Scholar 

  4. Betrand T., Jolivalt C., Briozzo P., Caminade E., Joly N., Madzak C. and Mougin C.2002. Crystal structure of a four-copper laccase complexed with an arylamine: Insights into substrate recognition and correlation with kinetics. Biochemistry41: 7325–7333.

    Article  CAS  Google Scholar 

  5. Bligny R. and Douce R.1983. Excretion of laccase by sycamore (Acer pseudoplatanus L.) cells. Purification and properties of the enzyme. Biochem. J.209: 489–496.

    PubMed  CAS  Google Scholar 

  6. Bruns T.D., Vilgalys R., Barns S.M., Gonzalez D., Hibbett D.S., Lane D.J., Simon L., Stickel S., Szaro T.M., Weisburg W.G. and Sogin M.L.1992. Evolutionary relationships within the fungi: analyses of nuclear small subunit rRNA sequences. Mol. Phylogenet. Evol.1: 231–241.

    PubMed  CAS  Article  Google Scholar 

  7. Calvo A.M., Copa-Patino J.L., Alonso O. and Gonzalez A.E.1998. Studies of the production and characterization of laccase activity in the basidiomycete Coriolopsis gallica, an efficient decolorizer of alkaline effluents. Arch. Microbiol.171: 31–36.

    PubMed  CAS  Article  Google Scholar 

  8. Choi G.H., Larson T.G. and Nuss D.L.1992. Molecular analysis of the laccase gene from the chestnut blight fungus and selective suppression of its expression in an isogenic hypovirulent strain. Mol. Plant. Microbe. Interact.5: 119–128.

    PubMed  CAS  Google Scholar 

  9. Dedeyan B., Klonowska A., Tagger S., Tron T., Iacazio G., Gil G. and Le Petit J.2000. Biochemical and molecular characterization of a laccase from Marasmius quercophilus. Appl. Environ. Microbiol.66: 925–929.

    PubMed  CAS  Article  Google Scholar 

  10. Diamantidis G., Effosse A., Potier P. and Bally R.2000. Purification and characterization of the first bacterial laccase in the rhizospheric bacterium Azospirillum lipoferum. Soil Biol. Biochem.32: 919–927.

    CAS  Article  Google Scholar 

  11. Ducros V., Brzozowski A.M., Wilson K.S., Brown S.H., Ostergaard P., Schneider P., Yaver D.S., Pedersen A.H. and Davies G.J.1998. Crystal structure of the type-2 depleted laccase from Coprinus cinereus at 2.2 A resolution. Nat. Struct. Biol.5: 310–316.

    PubMed  CAS  Article  Google Scholar 

  12. Eggert C., LaFayette P.R., Temp U., Eriksson K.E. and Dean J.F.1998. Molecular analysis of a laccase gene from the white rot fungus Pycnoporus cinnabarinus. Appl. Environ. Microbiol.64: 1766–1772.

    PubMed  CAS  Google Scholar 

  13. Felsenstein J.1989. PHYLIP–Phylogeny Inference Package (Version 3.2). Cladistics5: 164–166.

    Google Scholar 

  14. Ferandez-Larrea J. and Stahl U.1996. Isolation and characterization of a laccase gene from Podospora anserina. Mol. Gen. Genet.252: 539–551.

    Google Scholar 

  15. Genetics Computer Group 2002. Wisconsin Package Version 10.

  16. Germann U.A., Muller G.H.P.E. and Lerch K.1988. Characterization of two allelic forms of Neurospora crassa laccase. Amino-and carboxyl-terminal processing of a precursor. J. Biol. Chem.263: 885–896.

    PubMed  CAS  Google Scholar 

  17. Gianfreda L., Xu F. and Bollag J.-M.1999. Laccases: a useful group of oxidoreductive enzymes. Bioremediation J.3: 1–25.

    CAS  Article  Google Scholar 

  18. Giardina P., Aurilia V., Cannio R., Marzullo L., Amoresano A., Siciliano R., Pucci P. and Sannia G.1996. The gene, protein and glycan structures of laccase from Pleurotus ostreatus. Eur. J. Biochem.235: 508–515.

    PubMed  CAS  Article  Google Scholar 

  19. Giardina P., Cannio R., Martirani L., Marzullo L., Palmieri G. and Sannia G.1995. Cloning and sequencing of a laccase gene from the lignin-degrading basidiomycete Pleorotus ostreatus. Appl. Environ. Microbiol.61: 2408–2413.

    PubMed  CAS  Google Scholar 

  20. Giardina P., Palmieri G., Scaloni A., Fontanella B., Faraco V., Cennamo G. and Sannia G.1999. Protein and gene structure of a blue laccase from Pleurotus ostreatus. Biochem. J.341: 655–663.

    PubMed  CAS  Article  Google Scholar 

  21. Gomez-Alarcon G., Lahoz R. and Molina D.1989. Production of extracellular enzymes during growth and autolysis of Pycnoporus cinnabarinus. J. Basic Microbiol.29: 23–29.

    CAS  Google Scholar 

  22. Hatakka A.1994. Lignin-modifying enzymes from selected white-rot fungi, production and role in lignin degradation. FEMS Microbiol. Lett.13: 125–135.

    CAS  Article  Google Scholar 

  23. Henne A., Daniel R., Schmitz R.A. and Gottschalk G.1999. Construction of environmental DNA libraries in Escherichia coli and screening for the presence of genes conferring utilization of 4-hydroxybutyrate. Appl. Environ. Microbiol.65: 3901–3907.

    PubMed  CAS  Google Scholar 

  24. Hullo M.-F., Moszer I., Danchin A. and Martin-Verstraete I.2001. CotA of Bacillus subtilis is a copper-dependent enzyme. J. Bacteriol.183: 5426–5430.

    PubMed  CAS  Article  Google Scholar 

  25. Johannes C. and Majcherczyk A.2000. Laccase activity and laccase inhibitors. J. Biotechnol.78: 193–199.

    PubMed  CAS  Article  Google Scholar 

  26. Jonsson L.J., Saloheimo M. and Penttila M.1997. Laccase from the white-rot fungus Trametes versicolor: cDNA cloning of lcc1 and expression in Pichia patoris. Curr. Genet.32: 425–430.

    PubMed  CAS  Article  Google Scholar 

  27. Jonsson L., Sjöström K., Häggström I. and Nyman P.O.1995. Characterization of a laccase gene from the white-rot fungus Trametes versicolor and structural features of basidiomycete laccases. Biochim. Biophys. Acta1251: 210–215.

    PubMed  CAS  Google Scholar 

  28. Karahanian E., Corsini G., Lobos S. and Vicuna R.1998. Structure and expression of a laccase gene from the ligninoloytic basidiomycete Ceriporiopsis subvermispora. Biochim. Biophys. Acta1443: 65–74.

    PubMed  CAS  Google Scholar 

  29. Kojima Y., Tsukuda Y., Kawai Y., Tsukamoto A., Sugiura J., Sakaino M. and Kita Y.1990. Cloning, sequence analysis, and expression of ligninolytic phenoloxidase genes of the white-rot basidiomycete Coriolus hirsutus. J. Biol. Chem.265: 15224–15230.

    PubMed  CAS  Google Scholar 

  30. Kwon-Chung K.J. and Chang Y.C.1994. Gene arrangement and sequence of the 5S rRNA in Filobasidiella neoformans (Cryptococcus neoformans) as a phylogenetic indicator. Int. J. Syst. Bacteriol.44: 209–213.

    PubMed  CAS  Article  Google Scholar 

  31. Leonowicz A., Cho N.-S., Luterek J., Wilkolazka A., Wojtas-Wasilewska M., Matuszewska A., Hofrichter M., Wesenberg D. and Rogalski J.2001. Fungal laccase: properties and activity on lignin. J. Basic Microbiol.41: 185–227.

    PubMed  CAS  Article  Google Scholar 

  32. Litvintseva A.P. and Henson J.M.2002. Cloning, characterization, and transcription of three laccase genes from Gaeumannomyces graminis var. tritici, the take-all fungus. Appl. Environ. Microbiol.68: 1305–1311.

    PubMed  CAS  Article  Google Scholar 

  33. Mansur M., Suarez T., Ferandez-Larrea J., Brizuela M.A. and Gonzalez A.E.1997. Identification of a laccase gene family in the new lignin-degrading basidiomycete CECT 20197. Appl. Environ. Microbiol.63: 2637–2646.

    PubMed  CAS  Google Scholar 

  34. Mayer A.M.1987. Polyphenol oxidases in plants–recent progress. Phytochemistry26: 11–20.

    Article  Google Scholar 

  35. Mayer A.M. and Staples R.C.2002. Laccase: new functions for an old enzyme. Phytochemistry60: 551–565.

    PubMed  CAS  Article  Google Scholar 

  36. Messerschmidt A. and Huber R.1990. The blue oxidases, ascorbate oxidase, laccase and ceruloplasmin. Modelling and structural relationships. Eur. J. Biochem.187: 341–352.

    PubMed  CAS  Article  Google Scholar 

  37. Messerschmidt A., Ladenstein R., Huber R., Bolognesi M., Avigliano L., Petruzzelli R., Rossi A. and Finazzi-Agro A.1992. Refined crystal structure of ascorbate oxidase at 1.9 Å resolution. J. Mol. Biol.224: 179–205.

    PubMed  CAS  Article  Google Scholar 

  38. Messerschmidt A., Rossi A., Ladenstein R., Huber R., Bolognesi M., Gatti G., Marchesini A., Petruzzelli R. and Finazzi-Agro A.1989. X-ray crystal structure of the blue oxidase ascorbate oxidase from zucchini. Analysis of the polypeptide fold and a model of the copper sites and ligands. J. Mol. Biol.206: 513–529.

    PubMed  CAS  Article  Google Scholar 

  39. Mikuni J. and Morohoshi N.1997. Cloning and sequencing of a second laccase gene from the white-rot fungus Coriolus versicolor. FEMS Microbiol. Lett.155: 79–84.

    PubMed  CAS  Article  Google Scholar 

  40. Muñoz C., Guillén F., Martínez A.T. and Martínez M.J.1997. Induction and characterization of laccase in the ligninolytic fungus Pleurotus eryngii. Curr. Microbiol.34: 1–5.

    PubMed  Article  Google Scholar 

  41. Ong E., Pollock W.B. and Smith M.1997. Cloning and sequence of two laccase complementary DNAs from the ligninolytic basidiomycete Trametes versicolor. Gene196: 113–119.

    PubMed  CAS  Article  Google Scholar 

  42. Palmieri G., Giardina P., Bianco C., Fontanella B. and Sannia G.2000. Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl. Environ. Microbiol.66: 920–924.

    PubMed  CAS  Article  Google Scholar 

  43. Perry C.R., Smith M., Britnell C.H., Wood D.A. and Thurston C.F.1993. Identification of two laccase genes in the cultivated mushroom Agaricus bisporus. J. Gen. Microbiol.139: 1209–1218.

    PubMed  CAS  Google Scholar 

  44. Rogalski J., Lundell T., Leonowicz A. and Hatakka A.1991. Influence of aromatic compounds and lignin on production of ligninolytic enzymes by Phlebia radiata. Phytochemistry30: 2869–2872.

    CAS  Article  Google Scholar 

  45. Saloheimo M., Niku-Pavola M.L. and Knowles J.K.1991. Isolation and structural analysis of the laccase gene from the lignin-degrading fungus Phlebia radiata. J. Gen. Microbiol.137: 1537–1544.

    PubMed  CAS  Google Scholar 

  46. Sanchez-Amat A., Lucas-Elio P., Fernandez E., Garcia-Borron J.C. and Solano F.2001. Molecular cloning and functional characterization of a unique multipotent polyphenol oxidase from Marinomonas mediterranea. Biochim. Biophys. Acta1547: 104–116.

    PubMed  CAS  Google Scholar 

  47. Sato Y., Bao W., Sederoff R.R. and Whetten R.W.2001. Molecular cloning and expression of eight laccase cDNAs in loblolly pine (Pinus taeda). J. Plant. Res.114: 147–155.

    CAS  Article  Google Scholar 

  48. Smith M., Shnyreva A., Wood D.A. and Thurston C.F.1998. Tandem organization and highly disparate expression of the two laccase genes lcc1 and lcc2 in the cultivated mushroom Agaricus bisporus. Microbiology144: 1063–1069.

    PubMed  CAS  Article  Google Scholar 

  49. Soden D.M. and Dobson A.D.2001. Differential regulation of laccase gene expression in Pleurotus sajor-caju. Microbiology147: 1755–1763.

    PubMed  CAS  Google Scholar 

  50. Solomon E.I., Sundaraman U.M. and Machonkin T.E.1996. Multicopper oxidases and oxygenases. Chem. Rev.96: 2563–2605.

    PubMed  CAS  Article  Google Scholar 

  51. Tem U., Zierold U. and Eggert C.1999. Cloning and characterization of a second laccase gene from the lignin-degrading basidiomycete Pycnoporus cinnabarinus. Gene236: 169–177.

    Article  Google Scholar 

  52. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. and Higgins D.G.1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res.25: 4876–4882.

    PubMed  CAS  Article  Google Scholar 

  53. Wahleithner J.A., Xu F., Brown K.M., Golightly E.J., Halkier T., Kauppinen S., Pederson A. and Schneider P.1996. The identification and characterization of four laccases from the plant pathogenic fungus Rhizotocnia solani. Curr. Genet.29: 395–403.

    PubMed  CAS  Google Scholar 

  54. Williamson P.R.1994. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J. Bacteriol.176: 656–664.

    PubMed  CAS  Google Scholar 

  55. Xu F., Berka R.M., Wahleithner J.A., Nelson B.A., Shuster J.R., Brown S.H., Palmer A.E. and Solomon E.I.1998. Site-directed mutations in fungal laccase: Effect on redox potential, activity and pH profile. Biochem. J.334: 63–70.

    PubMed  CAS  Google Scholar 

  56. Xu F., Palmer A.E., Yaver D.S., Berka R.M., Gambetta G.A., Brown S.H. and Solomon E.I.1999. Targeted mutations in a Trametes villosa laccase. J. Biol. Chem.274: 12372–12375.

    PubMed  CAS  Article  Google Scholar 

  57. Yaver D.S. and Golightly E.J.1996. Cloning and characterization of three laccase genes from the white-rot basidiomycete Trametes villosa: genomic organization of the laccase gene family. Gene181: 95–102.

    PubMed  CAS  Article  Google Scholar 

  58. Yaver D.S., Overjero M.D., Xu F., Nelson B.A., Brown K.M., Halkier T., Bernauer S., Brown S.H. and Kauppinen S.1999. Molecular characterization of laccase genes from the basidiomycete Coprinus cinereus and heterologous expression of the laccase lcc1. Appl. Environ. Microbiol.65: 4943–4948.

    PubMed  CAS  Google Scholar 

  59. Yaver D.S., Xu F., Golightly E.J., Brown K.M., Brown S.H., Rey M.W., Schneider P., Halkier T., Mondorf K. and Dalboge H.1996. Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Appl. Environ. Microbiol.62: 834–841.

    PubMed  CAS  Google Scholar 

  60. Zhao J. and Kwan S.1999. Characterization, molecular cloning, and differential expression analysis of laccase genes from the edible mushroom Lentinula edodes. Appl. Environ. Microbiol.65: 4908–4913.

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Brenda Valderrama.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Valderrama, B., Oliver, P., Medrano-Soto, A. et al. Evolutionary and structural diversity of fungal laccases. Antonie Van Leeuwenhoek 84, 289–299 (2003). https://doi.org/10.1023/A:1026070122451

Download citation

  • Ascomycete
  • Basidiomycete
  • Laccase
  • Multi copper oxidases
  • White-rot fungi