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Bacterial laccases

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Abstract

Laccases (benzenediol oxygen oxidoreductases, EC 1.10.3.2) are polyphenol oxidases (PPO) that catalyze the oxidation of various substituted phenolic compounds by using molecular oxygen as the electron acceptor. The ability of laccases to act on a wide range of substrates makes them highly useful biocatalysts for various biotechnological applications. To date, laccases have mostly been isolated and characterized from plants and fungi, and only fungal laccases are used currently in biotechnological applications. In contrast, little is known about bacterial laccases, although recent rapid progress in the whole genome analysis suggests that the enzymes are widespread in bacteria. Since bacterial genetic tools and biotechnological processes are well established, so developing bacterial laccases would be significantly important. This review summarizes the distribution of laccases among bacteria, their functions, comparison with fungal laccases and their applications.

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References

  • Alexandre G, Zhulin LB (2000) Laccases are widespread in bacteria. Trends Biotechnol 18:41–42

    Article  PubMed  CAS  Google Scholar 

  • Alexandre G, Bally R, Taylor BL, Zhulin IB (1999) Loss of cytochrome oxidase activity and acquisition of resistance to quinone analogs in a laccase-positive variant of Azospirillum lipoferum. J Bacteriol 181:6730–6738

    PubMed  CAS  Google Scholar 

  • Arias ME, Arenas M, Rodríguez J, Soliveri J, Ball SA, Hernández M (2003) Kraft pulp biobleaching and mediated oxidation of a nonphenolic substrate by laccase from Streptomyces cyaneus CECT 3335. Appl Environ Microbiol 69:1953–1958

    Article  PubMed  CAS  Google Scholar 

  • Askwith C, Eide D, Van Ho A, Bernard PS, Li L, Davis-Kaplan S, Sipe DM, Kaplan J (1994) The FET3 gene of S. cerevisiae encodes a multi- copper oxidase required for ferrous iron uptake. Cell 76:403–410

    Article  PubMed  CAS  Google Scholar 

  • Bains J, Capalash N, Sharma P (2003) Laccase from a non- melanogenic, alkalotolerant γ-proteobacterium JB isolated from industrial waste water drained soil. Biotechnol Lett 25:1155–1159

    Article  PubMed  CAS  Google Scholar 

  • Baiocco P, Barreca AM, Fabbrini M, Galli C, Gentili P (2003) Promoting laccase activity towards non-phenolic substrates: a mechanistic investigation with some laccase-mediator systems. Org Biomol Chem 1:191–197

    Article  PubMed  CAS  Google Scholar 

  • Bertrand T, Jolivalt C, Briozzo P, Caminade E, Joly N, Madzak C, Mougin C (2002) Crystal structure of a four-copper laccase complexed with an arylamine: insights into substrate recognition and correlation with kinetics. Biochemistry 41:7325–7333

    Article  PubMed  CAS  Google Scholar 

  • Bligny R, Douce R (1983) Excretion of laccase by sycamore (Acer pseudoplatanus L.) cells. Purification and properties of the enzyme. J Biochem 204:489–496

    Google Scholar 

  • Bourbonnais R, Paice M (1990) Oxidation of non-phenolic substrates: An expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102

    Article  Google Scholar 

  • Bourbonnais RE, Paice MG (1992) Demethylation and delignification of kraft pulp by Trametes versicolor laccase in the presence of 2,2’-azinobis (3-ethylbenzthiazoline-6-sulphonate). Appl Microbiol Biotechnol 36:823–827

    Google Scholar 

  • Bourbonnais R, Paice MG (1996) Enzymatic delignification of Kraft pulp using laccase and a mediator. J Technol Assoc Pap Pulp Ind 79:199–204

    CAS  Google Scholar 

  • Brouwers GJ, de Vrind JPM, Corstjens PLAM, Cornelis P, Baysse C, de Vrind-deJong EW (1999) CumA, a gene encoding a multicopper oxidase, is involved in Mn -oxidation in Pseudomonas putida GB-1. Appl Environ Microbiol 65:1762–1768

    PubMed  CAS  Google Scholar 

  • Brown NL, Barrett SR, Camakaris J, Lee BT, Rouch DA (1995) Molecular gene and transport analysis of the copper resistance determinant (pco) from Escherichia coli plasmid pRJ 1004. Mol Microbiol 17:1153–1166

    Article  PubMed  CAS  Google Scholar 

  • Cai W, Martin R, Lemaure B, Leuba JL, Petiard V (1993) Hydroxy-indoles: a new class of laccase substrates. Plant Physiol Biochem 31:441–445

    CAS  Google Scholar 

  • Camarero S, Ibarra D, Martinez MJ, Martinez AT (2005) Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol 71:1775–1784

    Article  PubMed  CAS  Google Scholar 

  • Cha J, Cooksey DA (1991) Copper resistance in Pseudomonas syringae by periplasmic and outer membrane proteins. Proc Natl Acad Sci USA 88:8915–8919

    Article  PubMed  ADS  CAS  Google Scholar 

  • Chefetz B, Chen Y, Hadaar Y (1998) Purification and characterization of laccase from Chaetomium thermophillum and its role in humification. Appl Environ Microbiol 64:3175–3179

    PubMed  CAS  Google Scholar 

  • Claus H, Filip Z (1997) The evidence of a laccase-like activity in a Bacillus sphaericus strain. Microbiol Res 152:209–215

    CAS  Google Scholar 

  • Claus H, Faber G, Konig H (2002) Redox-mediated decolorization of synthetic dyes by fungal laccases. Appl Microbiol Biotechnol 59:672–678

    Article  PubMed  CAS  Google Scholar 

  • Claus H (2003) Laccases and their occurrence in prokayotes. Arch Microbiol 179:145–150

    PubMed  CAS  Google Scholar 

  • Deckert G, Warren PV, Gaasterland T, Young WG, Lenox AL, Graham DE, Overbeek R, Snead MA, Keller M, Aujay M, Huber R, Feldman RA, Short JM, Olson GJ, Swanson RV (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 393:353–358

    ADS  Google Scholar 

  • De Marco A, Roubelakis-Angelakis KA (1997) Laccase activity could contribute to cell-wall reconstitution in regenerating protoplasts. Phytochemistry 46:421–425

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Driks A (2004) The Bacillus subtilis spore coat. Phytopathology 94:1249–1251

    Article  CAS  Google Scholar 

  • Ducros V, Brzozowski AM, Wilson KS, Brown SH, Ostergaard P, Schneider P, Yaver DS, Pedersen AH, Davies GJ (1998) Crystal structure of the type-2 Cu depleted laccase from Coprinus cinereus at 2.2 Å resolution. Nat Struct Mol Biol 5:310–316

    Article  CAS  Google Scholar 

  • Eggert C, Temp U, Dean JFD, Eriksson KEL (1996) The lignolytic system of white rot fungus Pycnocarpus cinnabarinus: purification and characterization of the laccase. Appl Environ Microbiol 62:1151–1158

    PubMed  CAS  Google Scholar 

  • Endo K, Hayashi Y, Hibi T, Hosono K, Beppu T, Ueda K (2003) Enzymological characterization of Epo A, a laccase-like phenol oxidase produced by Streptomyces griseus. J Biochem 133:671–677

    Article  PubMed  CAS  Google Scholar 

  • Endo K, Hosono K, Beppu T, Ueda K (2002) A novel extracytoplasmic phenol oxidase of Streptomyces: its possible involvement in the onset of morphogenesis. Microbiology 148:1767–1776

    PubMed  CAS  Google Scholar 

  • Enguita JF, Martins OL, Henriques OA, Carrondo AM (2003) Crystal structure of a bacterial endospore coat component. J Biol Chem 278:19416–19425

    Article  PubMed  CAS  Google Scholar 

  • Faure D, Bouillant M, Bally R (1994) Isolation of Azospirillum lipoferum 4T Tn5 mutants affected in melanization and laccase activity. Appl Environ Microbiol 60:3413–3415

    PubMed  CAS  Google Scholar 

  • Faure D, Bouillant M, Bally R (1995) Comparative study of substrates and inhibitors of Azospirillum lipoferum and Pyricularia oryzae laccases. Appl Environ Microbiol 61:1144–1146

    PubMed  CAS  Google Scholar 

  • Fitz-Gibbon ST, Ladner H, Kim UJ, Stetter KO, Simon MI, Miller JH (2002) Genome sequence of the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. Proc Natl Acad Sci USA 99:984–989

    Article  PubMed  ADS  CAS  Google Scholar 

  • Francis CA, Tebo BM (2001) CumA multicopper oxidase genes from diverse Mn(II)-oxidizing and non-Mn(II)-oxidizing Pseudomonas strains. Appl Environ Microbiol 67:4272–4278

    Article  PubMed  CAS  Google Scholar 

  • Freeman JC, Nayar PG, Begley TP, Villafranca JJ (1993) Stoichiometry and spectroscopic identity of copper centers in phenoxazonine synthase: a new addition for the blue copper oxidase family. Biochemistry 32:4826–4830

    Article  PubMed  CAS  Google Scholar 

  • Froehner SC, Eriksson KE (1974) Purification and properties of Neurospora crassa laccase. J Bacteriol 120:458–465

    PubMed  CAS  Google Scholar 

  • Ghindilis AL, Gavrilova VP, Yaropolov AI (1992) Laccase-based biosensor for determination of polyphenols: determination of catechols in tea. Biosens Bioelectron 7:127–131

    Article  PubMed  Google Scholar 

  • Givaudan A, Effosse A, Faure D, Potier P, Bouillant ML, Bally R (1993) Polyphenol oxidase in Azospirillum lipoferum isolated from rice rhizosphere : evidence for laccase activity in nonmotile strains of Azospirillum lipoferum. FEMS Microbiol Lett 108:205–210

    Article  CAS  Google Scholar 

  • Hakulinen N, Kiiskinen LL, Kruus K, Saloheimo M, Paananen A, Koivula A, Rouvinen J (2002) Crystal structure of a laccase from Melanocarpus albomyces with an intact trinuclear copper site. Nat Struct Mol Biol 9:601–605

    CAS  Google Scholar 

  • Held C, Kandelbauer A, Schroeder M, Cavaco-Paulo A, Guebitz GM (2005) Biotransformation of phenolics with laccase-containing baterial spores. Environ Chem Lett 3:66–69

    Article  Google Scholar 

  • Hough MA, Hall JF, Kanbi LD, Hasnain SS (2001) Structure of the M148Q mutant of rusticyanin at 1.5A: a model for the copper site of stellacyanin. Acta Crystallogr 57:355–360

    CAS  Google Scholar 

  • Hullo MF, Moszer I, Danchin A, Martin-Verstraete I (2001) CotA of Bacillus subtilis is a copper-dependent laccase. J Bacteriol 183:5426–5430

    Article  PubMed  CAS  Google Scholar 

  • Huttermann A, Mai C, Kharazipour A (2001) Modification of lignin for the production of new compounded materials. Appl Microbiol Biotechnol 55:387–394

    Article  PubMed  CAS  Google Scholar 

  • Isono Y, Hoshino M (1989) Laccase-like activity of nucleoside oxidase in the presence of nucleosides. Agric Biol Chem 53:2197–2203

    CAS  Google Scholar 

  • Kawai S, Umezawa T, Shimada M, Higushi T (1988) Aromatic ring cleavage of 4,6-di(tert-butyl)guaiacol, a phenolic lignin model compound, by laccase of coriolus versicolor. FEBS Lett 236:309–311

    Article  PubMed  CAS  Google Scholar 

  • Kim C, Lorenz WW, Hoopes T, Dean JFD (2001) Oxidation of siderophores by the muticopper oxidase encoded by the Escherichia coli yac K gene. J Bacteriol 183:4866–4875

    Article  PubMed  CAS  Google Scholar 

  • Kumar SV, Phale PS, Durani S, Wangikar PP (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83:386–394

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Vanamala A, Kumar R (2005) Exploration of bacterial laccase in Pseudomonas stutzeri and its application in bleaching the wood pulp. FEBS J 272(s1)(N6-008P)

  • Lee Y, Hendson M, Panopoulos NJ, Schroth MN (1994) Molecular cloning, chromosomal mapping, and sequence analysis of copper resistance genes from Xanthomonas campestris pv. juglandis: homology with small copper proteins and multicopper oxidases. J Bacteriol 176:173–188

    PubMed  CAS  Google Scholar 

  • Lee FA, William CG (1987) Characterization of extracellular Mn2+-oxidizing protein from Leptothrix discophora SS-1. J Bacteriol 169: 1279–1285

    Google Scholar 

  • Lehman E, Harel E, Mayer AM (1974) Copper content and other characteristics of purified peach laccase. Phytochemistry 13:1713–1717

    Article  CAS  Google Scholar 

  • Malhotra K, Sharma P, Capalash N (2004) Copper and dyes enhance laccase production in γ-proteobacterim JB. Biotechnol Lett 26:1047–1050

    Article  PubMed  CAS  Google Scholar 

  • Mann KG, Jenny RJ, Krishnaswamy S (1988) Cofactor proteins in the assembly and expression of blood clotting enzyme complexes. Annu Rev Biochem 57:915–956

    Article  PubMed  CAS  Google Scholar 

  • Marbach I, Harel E, Mayer AM (1984) Molecular properties of extracelular Botrytis cinerea laccase. Phytochemistry 13:2713–2717

    Article  Google Scholar 

  • Martins LO, Soares CM, Pereira MM, Teixeira M, Costa T, Jones GH, Henriques AO (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 277:18849–18859

    Article  PubMed  CAS  Google Scholar 

  • Mayer AM (1987) Polyphenol oxidases in plants-recent progress. Phytochemistry 26:11–20

    Article  Google Scholar 

  • Mellano MA, Cooksey DA (1988) Nucleotide sequence and organization of copper resistance genes from Pseudomonas syringae pv.tomato. J Bacteriol 170:2879–2883

    PubMed  CAS  Google Scholar 

  • Messerschmidt A, Huber R (1990) The blue oxidases, ascorbate oxidase, laccase and ceruloplasmin. Eur J Biochem 187:341–352

    Article  PubMed  CAS  Google Scholar 

  • Miyazaki K (2005) A hyperthermophilic laccase from Thermus thermophilus HB27. Extremophiles 9:415–425

    Article  PubMed  CAS  Google Scholar 

  • Murugesan K (2003) Bioremediation of paper and pulp mill effluents. Indian J Exp Biol 41:1239–1248

    PubMed  CAS  Google Scholar 

  • Niku-Paavola Karhunen E, Salola P, Raunio V (1988) Lignolytic enzymes of the white rot fungus Phlebia radiata. J Biochem 254:877–884

    Google Scholar 

  • Okazaki M, Sugita T, Shimizu M, Ohode Y, Iwamoto K, de Vrind-deJong EW, de Vrind JPM, Corstjens PLAM (1997) Partial purification and characterization of mangenese-oxidizing factors of Pseudomonas fluorescens GB-1. Appl Environ Microbiol 63:4793–4799

    PubMed  CAS  Google Scholar 

  • Ouzounis C, Sander C (1991) A structure-derived sequence pattern for the detection of type I copper binding domains in distantly related proteins. FEBS Lett 279:73–78

    Article  PubMed  CAS  Google Scholar 

  • Palonen H, Viikari L (2004) Role of oxidative enzymatic treatments on enzymatic hydrolysis of softwood. Biotechnol Bioeng 86:550–557

    Article  PubMed  CAS  Google Scholar 

  • Peter MG, Wollenberger U (1997) Phenol-oxidizing enzymes: mechanisms and applications in biosensors. EXS 80:63–82

    PubMed  CAS  Google Scholar 

  • Ranocha P, McDougall G, Hawkins S, Sterjiades R, Borderies G, Stewart D, Cabanes-Macheteau M, Boudet AM, Goffner D (1999) Biochemical characterization, molecular cloning and expression of laccases—a divergent gene family in poplar. Eur J Biochem 259:485–495

    Article  PubMed  CAS  Google Scholar 

  • Reinhammar B (1984) Laccase. In: Lontie R (ed.) Copper proteins and copper enzymes, vol 3. CRC Press, Boca Raton, pp 1–35

    Google Scholar 

  • Roberts SA, Weichsel A, Grass G, Thakali K, Hazzard JT, Tollin G, Rensing C, Montfort WR (2002) Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc Natl Acad Sci USA 99:2766–2771

    Article  PubMed  ADS  CAS  Google Scholar 

  • Rogalski J, Lundell T, Leonowicz A, Hatakka A (1991) Production of laccase, lignin peroxidase and manganese-dependent peroxidase by various strains of Trametes versicolor depending on culture conditions. Acta Microbiol Pol 40:221–234

    CAS  Google Scholar 

  • Ruijssenaars HJ, Hartmans S (2004) A cloned Bacillus halodurans multicopper oxidase exhibiting alkaline laccase activity. Appl Microbiol Biotechnol 65:177–182

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Amat A, Solano F (1997) A pluripotent polyphenol oxidase from the melanogenic marine Altermonas sp. shares catalytic capabilities of tyrosinases and laccases. Biochem Biophys Res Commun 240:787–792

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Amat A, Lucas-Eilo P, Fernandez E, Garcia-Borron JC, Solano F (2001) Molecular cloning and functional characterization of a unique multipotent polyphenol oxidase from Marinomonas mediterranea. Biochim Biophys Acta 1547:104–116

    PubMed  CAS  Google Scholar 

  • Sannia G, Giardina P, Luna M, Rossi M, Buonocore V (1986) Laccase from Pleurotus ostreatus. Biotechnol Lett 8:797–800

    Article  CAS  Google Scholar 

  • Schneider P, Caspersen MB, Mondorf K, Halkier T, Skov LK, Østergaard PR, Brown KM, Brown SH, Xu F (1999) Characterization of a Coprinus cinereus laccase. Enzyme Microbial Technol 25:502–508

    Article  CAS  Google Scholar 

  • Solano F, Garcia E, Perez de Egea E, Sanchez-Amat A (1997) Isolation and characterization of strain MMB-1 a novel melanogenic marine bacterium. Appl Environ Microbiol 63: 3499–3506

    PubMed  CAS  Google Scholar 

  • Spillman A (2003) Enzyme may protect sugar beets from leaf spot disease. Agric Res 51:14

    Google Scholar 

  • Suzuki T, Endo K, Ito M, Tsujibo H, Miyamoto K, Inamori Y (2003) A thermostable laccase from Streptomyces lavendulae REN-7: purification, characterization, nucleotide sequence, and expression. Biosci Biotechnol Biochem 67:2167–2175

    Article  PubMed  CAS  Google Scholar 

  • Takami H, Takaki Y, Chee G (2002) Genome sequence of Oceanobacillus iheyensis isolated from the Iheya Ridge and its unexpected adaptive capabilities to extreme environments. Nucleic Acids Res 30:3927–3935

    Article  PubMed  CAS  Google Scholar 

  • Van Waasbergen LG, Hildebrand M, Tebo BM (1996) Identification and characterization of a gene cluster invoved in manganese oxidation by spores of a marine Bacillus sp strain SG-1 . J Bacteriol 178:3517–3530

    PubMed  Google Scholar 

  • Wesenberg D, Kyriakides I, Agathos SN (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187

    Article  PubMed  CAS  Google Scholar 

  • Wood DA (1980) Production, purification and properties of extracelluar laccase of Agaricus bisporus. J Gen Microbiol 117:327–338

    CAS  Google Scholar 

  • Xu F (1996) Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochemistry 35:7608–7614

    Article  PubMed  CAS  Google Scholar 

  • Xu F (2005) Applications of oxidoreductases: Recent progress. Ind Biotechnol 1:38–50

    Article  CAS  Google Scholar 

  • Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM, Solomon EL (1996) A study of a series of recombinant fungal laccases and bilirubin oxidase that exhibit significant differences in redox potential, substrate specificity, and stability. Biochim Biophys Acta 1292:303–311

    PubMed  Google Scholar 

  • Ygshinwa KK (2004) Japanese patent JP2004267177-A, Servicetech Japan

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  1. Department of Microbiology, Panjab University, Chandigarh, 160014, India

    P. Sharma & R. Goel

  2. Department of Biotechnology, Panjab University, Chandigarh, 160014, India

    N. Capalash

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  2. R. Goel
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Sharma, P., Goel, R. & Capalash, N. Bacterial laccases. World J Microbiol Biotechnol 23, 823–832 (2007). https://doi.org/10.1007/s11274-006-9305-3

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