Characterization of an alkali- and halide-resistant laccase expressed in E. coli: CotA from Bacillus clausii

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Brander, Søren ^a   Mikkelsen, Jørn D ^a   Kepp, Kasper P ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

COTA PROTEIN; LACCASE; UNCLASSIFIED DRUG; ALKALI; BACTERIAL PROTEIN; ENZYME INHIBITOR; HALOGEN; PYROGALLOL; PYROGALLOL 1,3-DIMETHYL ETHER; SODIUM CHLORIDE;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS; BACILLUS CLAUSII; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME METABOLISM; ENZYME STABILITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; MOLECULAR CLONING; NONHUMAN; PH; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; BACTERIAL GENE; CHEMICAL STRUCTURE; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; SEQUENCE HOMOLOGY; TEMPERATURE; TIME;

ALKALIES; BACILLUS; BACTERIAL PROTEINS; ENZYME ACTIVATION; ENZYME INHIBITORS; ENZYME STABILITY; ESCHERICHIA COLI; GENES, BACTERIAL; HALOGENS; HYDROGEN-ION CONCENTRATION; KINETICS; LACCASE; MODELS, MOLECULAR; PYROGALLOL; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM CHLORIDE; TEMPERATURE; TIME FACTORS;

EID: 84902589964     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099402     Document Type: Article

References (60)

1. Solomon EI, Sundaram UM, Machonkin TE (1996) Multicopper oxidases and oxygenases. Chem Rev 96: 2563-2606.
2. Solomon EI, Augustine AJ, Yoon J (2008) O2 reduction to H2O by the multicopper oxidases. Dalton Trans 30: 3921-3932.
3. Kunamneni A, Plou FJ, Ballesteros A, Alcalde M (2008) Laccases and their applications: A patent review. Recent patents on biotechnology 2: 10-24. (Pubitemid 351586673)
4. Rodgers CJ, Blanford CF, Giddens SR, Skamnioti P, Armstrong FA, et al. (2010) Designer laccases: a vogue for high-potential fungal enzymes? Trends Biotechnol 28: 63-72.
5. Riva S (2006) Laccases: Blue enzymes for green chemistry. Trends Biotechnol 24: 219-226.
6. Jia H, Zhong C, Huang F, Wang C, Jia L, et al. (2013) The preparation and characterization of a laccase nanogel and its application in naphthoquinone synthesis. ChemPlusChem 78: 451-458.
7. Torres-Salas P, Mate DM, Ghazi I, Plou FJ, Ballesteros AO, et al. (2013) Widening the pH activity profile of a fungal laccase by directed evolution. ChemBioChem 14: 934-937.
8. Sulistyaningdyah WT, Ogawa J, Tanaka H, Maeda C, Shimizu S (2004) Characterization of alkaliphilic laccase activity in the culture supernatant of Myrothecium verrucaria 24G-4 in comparison with bilirubin oxidase. FEMS Microbiol Lett 230: 209-214. (Pubitemid 38130203)
9. Singh G, Capalash N, Goel R, Sharma P (2007) A pH-stable laccase from alkalitolerant γ-proteobacterium JB: purification, characterization and indigo carmine degradation. Enzyme Microb Technol 41: 794-799. (Pubitemid 47361328)
10. Gunne M, Urlacher VB (2012) Characterization of the Alkaline Laccase Ssl1 from Streptomyces sviceus with Unusual Properties Discovered by Genome Mining. PLoS One 7(12): e52360.
11. Daâssi D, Zouari-Mechichi H, Prieto A, Martínez MJ, Nasri M, et al. (2013) Purification and biochemical characterization of a new alkali-stable laccase from Trametes sp. isolated in Tunisia: role of the enzyme in olive mill waste water treatment. World J Microbiol Biotechnol 29: 1-11.
12. Chen CY, Huang YC, Wei CM, Meng M, Liu WH, et al. (2013) Properties of the newly isolated extracellular thermo-alkali-stable laccase from thermophilic actinomycetes, Thermobifida fusca and its application in dye intermediates oxidation. AMB Express 3(1): 1-9.
13. Claus H (2003) Laccases and their occurrence in procaryotes. Arch Microbiol 179: 145-150.
14. Santhanam N, Vivanco JM, Decker SR, Reardon KF (2011) Expression of industrially relevant laccases: prokaryotic style. Trends Biotechnol 29(10): 480-489.
15. Martins LO, Soares CM, Pereira MM, Teixeira M, Costa T, et al. (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(21): 18849-18859. (Pubitemid 34952444)
16. Reiss R, Ihssen J, Richter M, Eichhorn E, Schilling B, et al. (2013) Laccase versus laccaselike multi-copper oxidase: A comparative study of similar enzymes with diverse substrate spectra. PLoS ONE 8(6): e65633.
17. Brissos V, Pereira L, Munteanu FD, Cavaco-Paulo A, Martins LO (2009) Expression system of CotA-laccase for directed evolution and high-throughput screenings for the oxidation of high-redox potential dyes. Biotechnol J 4(4): 558-563.
18. Sakasegawa SI, Ishikawa H, Imamura S, Sakuraba H, Goda S, et al. (2006) Bilirubin oxidase activity of Bacillus subtilis CotA. Appl Environm Microbiol 72(1): 972-975.
19. Fernandes AT, Damas JM, Todorovic S, Huber R, Baratto MC, et al. (2010) The multicopper oxidase from the archaeon Pyrobaculum aerophilum shows nitrous oxide reductase activity. FEBS J 277: 3176-3189.
20. Hullo MF, Moszer I, Danchin A, Martin-Verstraete I (2001) CotA of Bacillus subtilis is a copper-dependent laccase. J Bacteriol 183(18): 5426-5430. (Pubitemid 32802616)
21. Reiss R, Ihssen J, Thöny-Meyer L (2011) Bacillus pumilus laccase: a heat stable enzyme with a wide substrate spectrum. BMC Biotechnol 11(1): 9.
22. Ruijssenaars HJ, Hartmans S (2004) A cloned Bacillus halodurans multicopper oxidase exhibiting alkaline laccase activity. Appl Microbiol Biotechnol 65(2): 177-182. (Pubitemid 39062479)
23. Mohammadian M, Fathi-Roudsari M, Mollania N, Badoei-Dalfard A, Khajeh K (2010) Enhanced expression of a recombinant bacterial laccase at low temperature and microaerobic conditions: purification and biochemical characterization. J Industr Microbiol Biotechnol 37(8): 863-869.
24. Koschorreck K, Richter SM, Ene AB, Roduner E, Schmid RD, et al. (2008) Cloning and characterization of a new laccase from Bacillus licheniformis catalyzing dimerization of phenolic acids. Appl Microbiol Biotechnol 79(2): 217-224.
25. Telke AA, Ghodake GS, Kalyani DC, Dhanve RS, Govindwar SP (2011) Biochemical characteristics of a textile dye degrading extracellular laccase from a Bacillus sp. ADR. Biores Technol 102(2): 1752-1756.
26. Pan JB, Zhao M, Lu L, Du MH, Li GF, et al. (2011) Isolation and characterization of laccase activity in a novel Bacillus amyloliquefaciens LC02. Adv Mater Res 183: 773-777.
27. Kudanga T, Nugroho Prasetyo E, Sipilä J, Eberl A, Nyanhongo GS, et al. (2009) Coupling of aromatic amines onto syringylglycerol β-guaiacylether using Bacillus SF spore laccase: A model for functionalization of lignin-based materials. J Mol Catal B 61(3): 143-149.
28. Held C, Kandelbauer A, Schroeder M, Cavaco-Paulo A, Gübitz GM (2005) Biotransformation of phenolics with laccase containing bacterial spores. Environ Chem Lett 3(2): 74-77. (Pubitemid 41829690)
29. Dawkar VV, Jadhav UU, Jadhav SU, Govindwar SP (2008) Biodegradation of disperse textile dye Brown 3REL by newly isolated Bacillus sp. VUS. J Appl Microbiol 105(1): 14-24. (Pubitemid 351793562)
30. Abari AH, Emtiazi G, Roghanian R (2012) Production of none germinate spore ghost from a novel marine Bacillus with thermostable laccase activity. Afr J Microbiol Res 6(2): 393-402.
31. Zhang C, Diao H, Lu F, Bie X, Wang Y, et al. (2012) Degradation of triphenylmethane dyes using a temperature and pH stable spore laccase from a novel strain of Bacillus vallismortis. Biores Technol 126: 80-86.
32. Olukanni OD, Osuntoki AA, Awotula AO, Kalyani DC, Gbenle GO, et al. (2013) Decolorization of Dyehouse Effluent and Biodegradation of Congo Red by Bacillus thuringiensis RUN1. J Microbiol Biotechnol 23(6): 843-849.
33. Xu F (1997). Effects of redox potential and hydroxide inhibition on the pH activity profile of fungal laccases. J Biol Chem 272(2): 924-928.
34. Madzak C, Mimmi MC, Caminade E, Brault A, Baumberger S, et al. (2006) Shifting the optimal pH of activity for a laccase from the fungus Trametes versicolor by structure-based mutagenesis. Prot Eng Des Select 19(2): 77-84. (Pubitemid 43162259)
35. Durão P, Chen Z, Silva CS, Soares CM, Pereira MM, et al. (2008) Proximal mutations at the type 1 copper site of CotA laccase: spectroscopic, redox, kinetic and structural characterization of I494A and L386A mutants. Biochem J 412: 339-346.
36. Rodríguez Couto S, Toca Herrera JL (2006) Industrial and biotechnological applications of laccases: a review. Biotechnol Adv 24(5): 500-513. (Pubitemid 44082015)
37. Liu YH, Ye M, Lu Y, Zhang X, Li G (2011) Improving the decolorization for textile dyes of a metagenome-derived alkaline laccase by directed evolution. Appl Microbiol Biotechnol 91(3): 667-675.
38. Kageyama Y, Takaki Y, Shimamura S, Nishi S, Nogi Y, et al. (2007) Intragenomic diversity of the V1 regions of 16S rRNA genes in high-alkaline protease-producing Bacillus clausii spp. Extremophiles 11(4): 597-603. (Pubitemid 47012526)
39. Kobayashi T, Hakamada Y, Adachi S, Hitomi J, Yoshimatsu T, et al. (1995) Purification and properties of an alkaline protease from alkalophilic Bacillus sp. KSM-K16. Appl Microbiol Biotechnol 43(3): 473-481.
40. Durao P, Chen Z, Fernandes AT, Hildebrandt P, Murgida DH, et al. (2008) Copper incorporation into recombinant CotA laccase from Bacillus subtilis: characterization of fully copper loaded enzymes. J Biol Inorg Chem 13(2): 183-193. (Pubitemid 351172176)
41. Baril E, Coroller L, Couvert O, El Jabri M, Leguerinel I, et al. (2012) Sporulation boundaries and spore formation kinetics ofBacillus spp. as a function of temperature, pH and a(w). Food Microbiol 32(1): 79-86.
42. Anwar A, Saleemuddin M (1998) Alkaline proteases: a review. Biores Technol 64(3): 175-183. (Pubitemid 28327668)
43. Hall BG (2013) Building Phylogenetic Trees from Molecular Data with MEGA. Mol Biol Evol 30(5): 1229-1235.
44. Fernandes AT, Pereira MM, Silva CS, Lindley PF, Bento I, et al. (2011). The removal of a disulfide bridge in CotA-laccase changes the slower motion dynamics involved in copper binding but has no effect on the thermodynamic stability. J Biol Inorg Chem 16(4): 641-651.
45. Enguita FJ, Marçal D, Martins LO, Grenha R, Henriques AO, et al. (2004) Substrate and dioxygen binding to the endospore coat laccase from Bacillus subtilis. J Biol Chem 279: 23472-23476. (Pubitemid 38685658)
46. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protocols 4(3): 363-371.
47. Bond AM, Hollenkamp AF, Thompson SB, Bourne AR, Huf PA, et al. (1988) Analytical and mechanistic aspects of the electrochemical oxidation of keto steroids derivatized with phenylhydrazine,(4-nitrophenyl) hydrazine, and (2, 4-dinitrophenyl) hydrazine. Anal Chem 60(10): 1023-1027.
48. Sung YM, Gayam SR, Wu SP (2013) The oxidation of phenylhydrazine by tyrosinase. Appl Biochem Biotechnol 169(8): 2420-2429.
49. Costadinnova L, Hristova M, Kolusheva T, Stoilova N (2012) Conductometric study of the acidity properties of tannic acid (Chinese tannin). J Univ Chem Technol Metallurgy 47(3): 289-296.
50. Fawole OA, Makunga NP, Opara UL (2012) Antibacterial, antioxidant and tyrosinaseinhibition activities of pomegranate fruit peel methanolic extract. BMC Complement Altern Med 12(1): 200.
51. Giacomelli C, Ckless K, Galato D, Miranda FS, Spinelli A (2002) Electrochemistry of caffeic acid aqueous solutions with pH 2.0 to 8.5. J Braz Chem Soc 13(3): 332-338.
52. Hapiot P, Pinson J, Neta P, Rolando C (1993) Electrochemical behaviour of syringaldazine, a colorimetric redox reagent. J Electroanal Chem 353(1): 225-235.
53. Xu F, Shin W, Brown SH, Wahleithner JA, Sundaram UM, et al. (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 - Prot Struct Mol Enzymol 1292(2): 303-311.
54. Ferner-Ortner-Bleckmann J, Schrems A, Ilk N, Egelseer EM, Sleytr UB, et al. (2011) Multitechnique study on a recombinantly produced Bacillus halodurans laccase and an Slayer/laccase fusion protein. Biointerphases 6(2): 63-72.
55. Xu F, Berka RM, Wahleithner JA, Nelson BA, Shuster JR, et al. (1998) Site-directed mutations in fungal laccase: effect on redox potential, activity and pH profile. Biochem J 334: 63-70. (Pubitemid 28420972)
56. Naqui A, Varfolomeev SD (1980) Inhibition mechanism of Polyporus laccase by fluoride ion. FEBS Lett 113: 157-160.
57. Kittl R, Mueangtoom K, Gonaus C, Khazaneh ST, Sygmund C, et al. (2012) A chloride tolerant laccase from the plant pathogen ascomycete Botrytis aclada expressed at high levels in Pichia pastoris. J Biotechnol 157: 304-314.
58. Durand F, Kjaergaard CH, Suraniti E, Gounel S, Hadt RG, et al. (2012) Bilirubin oxidase from Bacillus pumilus: A promising enzyme for the elaboration of efficient cathodes in biofuel cells. Biosens Bioelectron 35(1): 140-146.
59. Mollania N, Khajeh K, Ranjbar B, Hosseinkhani S (2011) Enhancement of a bacterial laccase thermostability through directed mutagenesis of a surface loop. Enz Microb Technol 49(5): 446-452.
60. Mate DM, Gonzalez-Perez D, Falk M, Kittl R, Pia M, et al. (2013) Blood tolerant laccase by directed evolution. Chem Biol 20: 223-231.