New dye-decolorizing peroxidases from Bacillus subtilis and Pseudomonas putida MET94: Towards biotechnological applications

Applied Microbiology and Biotechnology

Volumn 98, Issue 5, 2014, Pages 2053-2065

  Santos, Ana ^a   Mendes, Sónia ^a   Brissos, Vânia ^a   Martins, Lígia O ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Bacillus subtilis; Dye decolorization; Dye decolorizing peroxidase; Phenols; Pseudomonas putida

Indexed keywords

BACILLUS SUBTILIS; BIOTECHNOLOGICAL APPLICATIONS; CHEMICAL DENATURATION; DYE DECOLORIZATION; DYE-DECOLORIZING PEROXIDASE; INDUSTRIAL BIOTECHNOLOGY; PSEUDOMONAS PUTIDA; SUBSTRATE SPECIFICITY;

AZO DYES; BACTERIA; BIOTECHNOLOGY; CLONING; ENZYME ACTIVITY; ESCHERICHIA COLI; OPTIMIZATION; PHENOLS; PLANTS (BOTANY); PORPHYRINS; REDOX REACTIONS; SUBSTRATES;

DYES;

AZO DYE; DYE DECOLORIZING PEROXIDASE; FERROUS ION; HEME; MANGANESE; PEROXIDASE; POLYMER; UNCLASSIFIED DRUG;

BIOTECHNOLOGY; CATALYSIS; DYE; ENZYME ACTIVITY; LIGNIN; OPTIMIZATION; PH; PHENOL; RECOMBINATION; SPECTROSCOPY; TEMPERATURE PROFILE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BIOTECHNOLOGY; CLONING; CONTROLLED STUDY; DECOLORIZATION; ESCHERICHIA COLI; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PH; PROTEIN ENGINEERING; PSEUDOMONAS PUTIDA;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS PUTIDA;

BACILLUS SUBTILIS; CLONING, MOLECULAR; COLORING AGENTS; ENZYME STABILITY; ESCHERICHIA COLI; GENE EXPRESSION; HYDROGEN-ION CONCENTRATION; MOLECULAR WEIGHT; PEROXIDASES; PROTEIN MULTIMERIZATION; PSEUDOMONAS PUTIDA; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 84896691646     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5041-4     Document Type: Article

References (50)

1. Ahmad M, Roberts JN, Hardiman EM, Singh R, Eltis LD, Bugg TD (2011) Identification of DypB from Rhodococcus jostii RHA1 as a lignin peroxidase. Biochemistry 50:5096-5107
2. Ayala M (2010) Redox potential of peroxidases. Springer, Heidelberg
3. Banci L, Bertini I, Turano P, Tien M, Kirk TK (1991) Proton NMR investigation into the basis for the relatively high redox potential of lignin peroxidase. Proc Natl Acad Sci U S A 88:6956-6960 (Pubitemid 21915068)
4. Berry EA, Trumpower BL (1987) Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 161:1-15
5. Brown ME, Barros T, Chang MC (2012) Identification and characterization of a multifunctional dye peroxidase from a lignin-reactive bacterium. ACS Chem Biol 7:2074-2081
6. 2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 65:857-875
7. Chung N, Aust SD (1995) Veratryl alcohol-mediated indirect oxidation of phenol by lignin peroxidase. Arch Biochem Biophys 316:733-737
8. Durão P, Bento I, Fernandes AT, Melo EP, Lindley PF, Martins LO (2006) Perturbations of the T1 copper site in the CotA laccase from Bacillus subtilis: structural, biochemical, enzymatic and stability studies. J Biol Inorg Chem 11:514-526
9. Fernandes AT, Martins LO, Melo EP (2009) The hyperthermophilic nature of the metallo-oxidase from Aquifex aeolicus. Biochim Biophys Acta 1794:75-83
10. Hewson WD, Hager LP (1979) Oxidation of horseradish peroxidase compound II to compound I. J Biol Chem 254:3182-3186
11. Hiner AN, Hernandez-Ruiz J, Rodriguez-Lopez JN, Garcia-Canovas F, Brisset NC, Smith AT, Arnao MB, Acosta M (2002) Reactions of the class II peroxidases, lignin peroxidase and Arthromyces ramosus peroxidase, with hydrogen peroxide. Catalase-like activity, compound III formation, and enzyme inactivation. J Biol Chem 277:26879-26885 (Pubitemid 34951696)
12. Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biotechnol 87:871-897
13. Jongbloed JD, Grieger U, Antelmann H, Hecker M, Nijland R, Bron S, van Dijl JM (2004) Two minimal Tat translocases in Bacillus. Mol Microbiol 54:1319-1325 (Pubitemid 39578274)
14. Kandelbauer A, Gübitz GM (2005) Bioremediation for the decolorization of textile dyes - a review. In: Lichtfouse E, Schwarzbauer J, Robert D (eds) Environmental chemistry. Springer, Berlin, pp 269-288
15. Kelley LA, Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363-371
16. Kim SJ, Shoda M (1999) Purification and characterization of a novel peroxidase from Geotrichum candidum dec 1 involved in decolorization of dyes. Appl Environ Microbiol 65:1029-1035 (Pubitemid 29111167)
17. Krishnappa L, Monteferrante CG, van Dijl JM (2012) Degradation of the twin-arginine translocation substrate YwbN by extracytoplasmic proteases of Bacillus subtilis. Appl Environ Microbiol 78:7801-7804
18. Kuan I-C, Johnson K, Tien M (1993) Kinetic analysis of manganese peroxidase. J Biol Chem 268:20064-20070
19. Liers C, Bobeth C, Pecyna M, Ullrich R, Hofrichter M (2010) DyP-like peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes. Appl Microbiol Biotechnol 85:1869-1879
20. Liers C, Ullrich R, Hofrichter M, Minibayeva FV, Beckett RP (2011) A heme peroxidase of the ascomyceteous lichen Leptogium saturninum oxidizes high-redox potential substrates. Fungal Genet Biol 48:1139-1145
21. Liu X, Du Q, Wang Z, Zhu D, Huang Y, Li N, Wei T, Xu S, Gu L (2011) Crystal structure and biochemical features of EfeB/YcdB from Escherichia coli O157: ASP235 plays divergent roles in different enzyme-catalyzed processes. J Biol Chem 286:14922-14931
22. Martinez AT, Ruiz-Duenas FJ, Martinez MJ, Del Rio JC, Gutierrez A (2009) Enzymatic delignification of plant cell wall: from nature to mill. Curr Opin Biotechnol 20:348-357
23. 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 (Pubitemid 34952444)
24. Mendes S, Farinha A, Ramos CG, Leitao JH, Viegas CA, Martins LO (2011a) Synergistic action of azoreductase and laccase leads to maximal decolourization and detoxification of model dye-containing wastewaters. Bioresour Technol 102:9852-9859
25. Mendes S, Pereira L, Batista C, Martins LO (2011b) Molecular determinants of azo reduction activity in the strain Pseudomonas putida MET94. Appl Microbiol Biotechnol 92:393-405
26. Ogola HJ, Kamiike T, Hashimoto N, Ashida H, Ishikawa T, Shibata H, Sawa Y (2009) Molecular characterization of a novel peroxidase from the cyanobacterium Anabaena sp. strain PCC 7120. Appl Environ Microbiol 75:7509-7518
27. Pereira L, Coelho A, Viegas AC, Ganachaud C, Lacazio G, Tron T, Robalo M, Martins LO (2009a) On the mechanism of biotransformation of the anthraquinonic dye Acid Blue 62 by laccases. Adv Synth Catal 351:1857-1865
28. Pereira L, Coelho AV, Viegas CA, Santos MM, Robalo MP, Martins LO (2009b) Enzymatic biotransformation of the azo dye sudan orange G with bacterial CotA-laccase. J Biotechnol 139:68-77
29. Poulos TL, Kraut J (1980) The stereochemistry of peroxidase catalysis. J Biol Chem 255:8199-8205
30. Roberts JN, Singh R, Grigg JC, Murphy ME, Bugg TD, Eltis LD (2011) Characterization of dye-decolorizing peroxidases from Rhodococcus jostii RHA1. Biochemistry 50:5108-5119
31. Rodriguez-Couto S (2009) Enzymatic biotransformation of synthetic dyes. Curr Drug Metab 10:1048-1054
32. Ruiz-Duenas FJ, Martinez AT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microbiol Biotechnol 2:164-177
33. Scheibner M, Hulsdau B, Zelena K, Nimtz M, de Boer L, Berger RG, Zorn H (2008) Novel peroxidases of Marasmius scorodonius degrade β-carotene. Appl Microbiol Biotechnol 77:1241-1250
34. Sezer S, Genebra T, Mendes S, Martins LO, Todorovic S (2012) A DyP-type peroxidase at a bio-compatible interface: structural and mechanistic insights. Soft Matter 8:10314-10321
35. Sezer S, Santos A, Kielb P, Pinto T, Martins LO, Todorovic S (2013) Distinct structural and redox properties of heme active in bacterial DyP-type peroxidases from two subfamilies: resonance Raman and electrochemistry study. Biochemistry 52:3074-3084
36. Singh R, Grigg JC, Armstrong Z, Murphy ME, Eltis LD (2012) Distal heme pocket residues of B-type dye-decolorizing peroxidase: arginine but not aspartate is essential for peroxidase activity. J Biol Chem 287:10623-10630
37. Strittmatter E, Liers C, Ullrich R, Wachter S, Hofrichter M, Plattner DA, Piontek K (2012) First crystal structure of a fungal high-redox potential dye-decolorizing peroxidase: substrate interaction sites and long-range electron transfer. J Biol Chem 288:4095-4102
38. Sturm A, Schierhorn A, Lindenstrauss U, Lilie H, Bruser T (2006) YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins. J Biol Chem 281:13972-13978 (Pubitemid 43848323)
39. Sugano Y (2009) DyP-type peroxidases comprise a novel heme peroxidase family. Cell Mol Life Sci 66:1387-1403
40. Sugano Y, Matsushima Y, Shoda M (2006) Complete decolorization of the anthraquinone dye reactive blue 5 by the concerted action of two peroxidases from Thanatephorus cucumeris Dec 1. Appl Microbiol Biotechnol 73:862-871 (Pubitemid 44833031)
41. Sugano Y, Muramatsu R, Ichiyanagi A, Sato T, Shoda M (2007) DyP, a unique dye-decolorizing peroxidase, represents a novel heme peroxidase family: ASP171 replaces the distal histidine of classical peroxidases. J Biol Chem 282:36652-36658
42. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
43. Valderrama B, Ayala M, Vazquez-Duhalt R (2002) Suicide inactivation of peroxidases and the challenge of engineering more robust enzymes. Chem Biol 9:555-565 (Pubitemid 34593036)
44. van Bloois E, Torres Pazmino DE, Winter RT, Fraaije MW (2010) A robust and extracellular heme-containing peroxidase from Thermobifida fusca as prototype of a bacterial peroxidase superfamily. Appl Microbiol Biotechnol 86:1419-1430
45. van der Ploeg R, Barnett JP, Vasisht N, Goosens VJ, Pother DC, Robinson C, van Dijl JM (2011) Salt sensitivity of minimal twin arginine translocases. J Biol Chem 286:43759-43770
46. van der Ploeg R, Monteferrante CG, Piersma S, Barnett JP, Kouwen TR, Robinson C, van Dijl JM (2012) High-salinity growth conditions promote Tat-independent secretion of Tat substrates in Bacillus subtilis. Appl Environ Microbiol 78:7733-7744
47. Wong DW (2009) Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol 157:174-209
48. Yoshida T, Tsuge H, Konno H, Hisabori T, Sugano Y (2011) The catalytic mechanism of dye-decolorizing peroxidase DyP may require the swinging movement of an aspartic acid residue. FEBS J 278:2387-2394
49. Zubieta C, Joseph R, Krishna SS, McMullan D, Kapoor M, Axelrod HL, Miller MD, Abdubek P, Acosta C, Astakhova T, Carlton D, Chiu HJ, Clayton T, Deller MC, Duan L, Elias Y, Elsliger MA, Feuerhelm J, Grzechnik SK, Hale J, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Kumar A, Marciano D, Morse AT, Murphy KD, Nigoghossian E, Okach L, Oommachen S, Reyes R, Rife CL, Schimmel P, Trout CV, van den Bedem H, Weekes D, White A, Xu Q, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson IA (2007a) Identification and structural characterization of heme binding in a novel dye-decolorizing peroxidase, TyrA. Proteins 69:234-243 (Pubitemid 47429287)
50. Zubieta C, Krishna SS, Kapoor M, Kozbial P, McMullan D, Axelrod HL, Miller MD, Abdubek P, Ambing E, Astakhova T, Carlton D, Chiu HJ, Clayton T, Deller MC, Duan L, Elsliger MA, Feuerhelm J, Grzechnik SK, Hale J, Hampton E, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kumar A, Marciano D, Morse AT, Nigoghossian E, Okach L, Oommachen S, Reyes R, Rife CL, Schimmel P, van den Bedem H, Weekes D, White A, Xu Q, Hodgson KO, Wooley J, Deacon AM, Godzik A, Lesley SA, Wilson IA (2007b) Crystal structures of two novel dye-decolorizing peroxidases reveal a β-barrel fold with a conserved heme-binding motif. Proteins 69:223-233 (Pubitemid 47429286)