Phenol-oxidizing laccases from the termite gut

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 10, 2010, Pages 723-732

  Coy, M R ^a   Salem, T Z ^a   Denton, J S ^a   Kovaleva, E S ^b   Liu, Z ^b   Barber, D S ^a   Campbell, J H ^b   Davis, D C ^b   Buchman, G W ^b   Boucias, D G ^a   Scharf, M E ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b Chesapeake PERL Inc   (United States)

Author keywords

Bioethanol; Laccase; Lignin; Lignocellulose; Phenoloxidase; Termite

Indexed keywords

INSECT PROTEIN; LACCASE; PHENOL;

ANIMAL; ARTICLE; CLASSIFICATION; ENZYMOLOGY; GENETICS; INTESTINE; ISOPTERA; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY;

ANIMALS; INSECT PROTEINS; INTESTINES; ISOPTERA; LACCASE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHENOL; PHYLOGENY;

EUKARYOTA; HEXAPODA; ISOPTERA; PROKARYOTA; RETICULITERMES FLAVIPES;

EID: 77957000044     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.07.004     Document Type: Article

References (59)

1. Aiba H., Yokoyama A., Tanaka H. Copper(II) complexes of histidine and its related compounds in aqueous solutions. Bull. Chem. Soc. Jpn. 1974, 47:1003-1007.
2. Arakane Y., Muthukrishnan S., Beeman R.W., Kanost M.R., Kramer K.J. Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc. Natl. Acad. Sci. USA 2005, 103:11337-11342.
3. Baldrian P. Fungal laccases - occurrence and properties. FEMS Microbiol. Rev. 2006, 30:215-242.
4. Britton H.T.S., Robinson R.A. Universal buffer solutions and dissociation constant of veronal. J. Chem. Soc. 1931, 1456-1462.
5. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides, SignalP 3. 0. J. Mol. Biol. 2004, 340:783-795.
6. Breznak J.A., Brune A. Role of microorganisms in the digestion of lignocellulose by termites. Annu. Rev. Entomol. 1994, 39:453-487.
7. Brune A., Emerson D., Breznak J.A. The termite gut microflora as an oxygen sink, microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl. Environ. Microbiol. 1995, 61:2681-2687.
8. Brune A., Miambi E., Breznak J.A. Roles of oxygen and the intestinal microflora in the metabolism of lignin-derived phenylpropanoids and other monoaromatic compounds by termites. Appl. Environ. Microbiol. 1995, 61:2688-2695.
9. Bryant D., Moulton V. Neighbor-Net, an agglomerative method for the construction of phylogenetic networks. Mol. Biol. Evol. 2004, 21:255-265.
10. Butler J.H.A., Buckerfield J.C. Digestion of lignin by termites. Soil Biol. Biochem. 1979, 11:507-511.
11. Call H.P., Mucke I. History, overview and applications of mediated ligninolytic system, especially laccase mediator system (lignozym-process). J. Biotechnol. 1997, 53:163-202.
12. Canters G.W., Gilardi G. Engineering type 1 copper sites in proteins. FEBS Lett. 1993, 325:39-48.
13. Chance B., Maehly A.C. Assay of catalase and peroxidases. Meth. Enzymol. 1955, 2:764-775.
14. Cookson L.J. 14C-lignin degradation by three Australian termite species. Wood Sci. Technol. 1987, 21:11-25.
15. Cookson L.J. The site and mechanism of 14C-lignin degradation by Nasutitermes exitosus. J. Insect Physiol. 1988, 34:409-414.
16. Dittmer N.T., Gorman M.J., Kanost M.R. Characterization of endogenous and recombinant forms of laccase-2, a multicopper oxidase from the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 2009, 39:596-606.
17. Dittmer N.T., Kanost M.R. Insect multicopper oxidases: diversity, properties, and physiological roles. Insect Biochem. Mol. Biol. 2010, 40:179-188.
18. Dittmer N.T., Suderman R.J., Jiang H., Zhu Y.C., Gorman M.J., Kramer K.J., Kanost M.R. Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae. Insect Biochem. Mol. Biol. 2004, 34:29-41.
19. Edgar R.C. MUSCLE, multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
20. Esenther G.R., Kirk T.K. Catabolism of aspen sapwood in Reticulitermes flavipes. Ann. Entomol. Soc. Am. 1974, 67:989-991.
21. Geib S.M., Filley T.R., Hatcher P.G., Hoover K., Carlson J.E., Jimenez-Gasco M.M., Nakagawa-Izumi A., Sleighter R.L., Tien M. Lignin degradation in wood-feeding insects. Proc. Natl. Acad. Sci. USA 2008, 105:12932-12937.
22. Goloboff P.A., Farris J.S., Nixon K.C. TNT, a free program for phylogenetic analysis. Cladistics 2008, 24:774-786.
23. Gorman M.J., Dittmer N.T., Marshall J.L., Kanost M.R. Characterization of the multicopper oxidase gene family in Anopheles gambiae. Insect Biochem. Mol. Biol. 2008, 38:817-824.
24. Harkin J.M., Larsen M.J., Obst J.R. Use of syringaldazine for detection of laccase in sporophores of wood rotting fungi. Mycologia 1974, 66:469-476.
25. Hernández M., Hernández-Coronado M.J., Ball A.S., Arias M.E. Degradation of alkali-lignin residues from solid-state fermentation of wheat straw by streptomycetes. Biodegradation 2001, 12:219-223.
26. Huson D.H., Bryant D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006, 23:254-267.
27. Humphreys J.M., Hemm M.R., Chapple C. New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc. Natl. Acad. Sci. U S A 1999, 96:10045-10050.
28. Itakura S., Ueshima K., Tanaka H., Enoki A. Degradation of wood components by subterranean termite. Coptotermes formosanus. Mokuzai Gakkaishi 1995, 41:580-586.
29. Johannes C., Majcherczyk A. Natural mediators in the oxidation of polycyclic aromatic hydrocarbons by laccase mediator systems. Appl. Environ. Microbiol. 2000, 66:524-528.
30. Katsumata K.S., Jin Z., Hori K., Iiyama K. Structural changes in lignin of tropical woods during digestion by termite, Cryptotermes brevis. J. Wood Sci. 2007, 53:419-426.
31. Kiiskinen L.L., Viikari L., Kruus K. Purification and characterisation of a novel laccase from the ascomycete Melanocarpus albomyces. Appl. Microbiol. Biotechnol. 2002, 59:198-204.
32. Kovaleva E.S., O'Connell K.P., Buckley P., Liu Z., Davis D.C. Recombinant protein production in insect larvae, host choice, tissue distribution, and heterologous gene instability. Biotechnol. Lett. 2009, 31:381-386.
33. Kuhnigk T., König H. Degradation of dimeric lignin model compounds by aerobic bacteria isolated from the hindgut of xylophagous termites. J. Basic Microbiol. 1997, 37:205-211.
34. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (Delta Delta C(T)) method. Methods 2001, 25:402-408.
35. Maddison, W.P., and Maddison, D.R., (2008). MESQUITE, a Modular System for Evolutionary Analysis, Version 2.5.
36. Matsui T., Tokuda G., Shinzato N. Termites as functional gene resources. Recent Pat. Biotechnol. 2009, 3:10-18.
37. Messerschmidt A. Multi-copper Oxidases 1997, World Scientific Pub Co Inc., Singapore.
38. Messerschmidt A., Huber R. The blue oxidases, ascorbate oxidase, laccase and ceruloplasmin. Modelling and structural relationships. Eur. J. Biochem. 1990, 187:341-352.
39. Min K.L., Kim Y.H., Kim Y.W., Jung H.S., Hah Y.C. Characterization of a novel laccase produced by the wood-rotting fungus Phellinus ribis. Arch. Biochem. Biophys. 2001, 392:279-286.
40. Nakamura K., Go N. Function and molecular evolution of multicopper blue proteins. Cell. Mol. Life Sci. 2005, 62:2050-2066.
41. O'Connell K.P., Kovaleva E., Campbell J.H., Anderson P.E., Brown S.G., Davis D.C., Valdes J.J., Welch R.W., Bentley W.E., van Beek N.A. Production of a recombinant antibody fragment in whole insect larvae. Mol. Biotechnol. 2007, 36:44-51.
42. Ohkuma M. Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl. Microbiol. Biotechnol. 2003, 61:1-9.
43. Palmieri G., Giardina P., Bianco C., Fontanella B., Sannia G. Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl. Environ. Microbiol. 2000, 66:920-924.
44. Palmieri G., Giardina P., Bianco C., Scaloni A., Capasso A., Sannia G. A novel white laccase from Pleurotus ostreatus. J. Biol. Chem. 1997, 272:31301-31307.
45. Perrin D.D. Histidine-copper (II) complexes. Nature 1959, 184:1868-1869.
46. Ponting C.P., Schultz J., Milpetz F., Bork P. SMART, identification and annotation of domains from signalling and extracellular protein sequences. Nucleic Acids Res. 1999, 27:229-232.
47. Scharf M.E., Tartar A. Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod. Bioref. 2008, 2:540-552.
48. Scharf M.E., Kovaleva E.S., Jadhao S., Campbell J.H., Buchman G.W., Boucias D.G. Functional and translational analyses of a beta-glucosidase gene (glycosyl hydrolase family 1) isolated from the gut of the lower termite Reticulitermes flavipes. Insect Biochem. Mol. Biol. 2010, 40:611-620.
49. Solomon E.I., Chen P., Metz M., Lee S.K., Palmer A.E. Oxygen binding, activation, and reduction to water by copper proteins. Angew. Chem. Int. Ed. Engl. 2001, 40:4570-4590.
50. Solomon E.I., Sundaram U.M., Machonkin T.E. Multicopper oxidases and oxygenases. Chem. Rev. 1996, 96:2563-2606.
51. Suderman R.J., Dittmer N.T., Kanost M.R., Kramer K.J. Model reactions for insect cuticle sclerotization, cross-linking of recombinant cuticular proteins upon their laccase-catalyzed oxidative conjugation with catechols. Insect Biochem. Mol. Biol. 2006, 36:353-365.
52. Tartar A., Wheeler M.M., Zhou X., Coy M.R., Boucias D.G., Scharf M.E. Parallel meta-transcriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnol. Biofuels 2009, 2:25.
53. Wang M., Feng W.Y., Zhao Y.L., Chai Z.F. ICP-MS-based strategies for protein quantification. Mass Spec. Rev. 2009, 10.1002/mas.20241.
54. Whelan S., Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 2001, 18:691-699.
55. Xu F., Shin W., Brown S.H., Wahleithner J.A., Sundaram U.M., Solomon E.I. 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 1996, 1292:303-311.
56. Yatsu J., Asano T. Cuticle laccase of the silkworm, Bombyx mori, Purification, gene identification and presence of its inactive precursor in the cuticle. Insect Biochem. Mol. Biol. 2009, 39:254-262.
57. Zhou X., Smith J.A., Oi F.M., Koehler P.G., Bennett G.W., Scharf M.E. Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite Reticulitermes flavipes. Gene 2007, 395:29-39.
58. Zhou X., Kovaleva E.S., Wu-Scharf D., Campbell J.H., Buchman G.W., Boucais D.G., Scharf M.E. Production and characterization of a recombinant beta-1, 4 endoglucanase (glycohydrolase family 9) from the termite Reticulitermes flavipes. Arch. Insect Biochem. Physiol 2010, 74:147-162.
59. Zoroddu M.A., Medici S., Peana M. Copper and nickel binding in multi-histidinic peptide fragments. J. Inorg. Biochem. 2009, 103:1214-1220.