Skip to main content
SpringerLink
Log in

Degradation pathway of an anthraquinone dye catalyzed by a unique peroxidase DyP from Thanatephorus cucumeris Dec 1

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

The reactants produced by action of a purified unique dye-decolorizing peroxidase, DyP, on a commercial anthraquinone dye, Reactive Blue 5, were investigated using electrospray ionization mass spectrometry (ESI-MS), thin-layer chromatography (TLC), and 1H- and 13C- nuclear magnetic resonance (NMR). The results of ESI-MS analysis showed that phthalic acid, a Product 2 (molecular weight 472.5), and a Product 3 (molecular weight 301.5), were produced. Product 2 and Product 3 were generated by usual peroxidase reaction, whereas phthalic acid was generated by hydrolase- or oxygenase-catalyzed reaction. One potential associated product, o-aminobenzene sulfonic acid, was found to be converted to 2,2′-disulfonyl azobenzene by ESI-MS and NMR analyses. From these results, we propose, for the first time, the degradation pathway of an anthraquinone dye by the enzyme DyP.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alva KS, Kumar J, Marx KA, Tripathy SK (1997) Enzymatic synthesis and characterization of a novel water-soluble polyaniline: poly (2,5-diaminobenzenesulfonate). Macromolecules 30:4024–4029. doi:10.1021/ma961544h

    Article  CAS  Google Scholar 

  • Anliker R (1979) Ecotoxicology of dyestuffs—a joint effort by industry. Ecotoxicol Environ Saf 3:59–74. doi:10.1016/0147-6513(79)90060-5

    Article  PubMed  CAS  Google Scholar 

  • Banat IM, Nigam P, Singh D, Marchant R (1996) Microbial decolorization of textile-dye-containing effluents. Bioresour Technol 58:217–227. doi:10.1016/S0960-8524(96)00113-7

    Article  CAS  Google Scholar 

  • Cartoni A, Menna P, Salvatorelli E, Braghiroli D, Giampietro R, Animati F, Urabani A, Boccio PD, Minotti G (2004) Oxidative degradation of cardiotoxic anticancer anthracyclines to phthalic acids. J Biol Chem 279:5088–5099. doi:10.1074/jbc.M306568200

    Article  PubMed  CAS  Google Scholar 

  • Chivukula M, Spadaro JT, Renganathan V (1995) Lignin peroxidase catalized oxidation of sulfonated azo dyes generates novel sulfophenyl hydroperoxides. Biochemistry 34:7765–7772. doi:10.1021/bi00023a024

    Article  PubMed  CAS  Google Scholar 

  • Chung KT, Stevens E Jr (1993) Degradation of azo dyes by environmental microorganisms and heliminths. Environ Toxicol Chem 12:2121–2132. doi:10.1897/1552-8618(1993)12[2121:DOADBE]2.0.CO;2

    Article  CAS  Google Scholar 

  • Dunford HB (1999) Heme peroxidases. Wiley-VCH, New York

    Google Scholar 

  • Fang H, Wenrong H, Yuezhong L (2004) Biodegradation mechanisms and kineteics of azo dye 4BS by a microbial consortium. Chemosphere 57:293–301. doi:10.1016/j.chemosphere.2004.06.036

    Article  CAS  Google Scholar 

  • Fu Y, Viraraghavan T (2001) Fungal decolorization of dye wastewaters—a review. Bioresour Technol 79:251–262. doi:10.1016/S0960-8524(01)00028-1

    Article  PubMed  CAS  Google Scholar 

  • Goszczynski S, Paszczynski A, Pasti-Grigsby MB, Crawford RL, Crawford DL (1994) New pathway for degradation of sulfonated azo dyes by microbial peroxidases of Phanerochaete chrysosporium and Streptomyces chromofuscus. J Bacteriol 176:1339–1347

    PubMed  CAS  Google Scholar 

  • Heinfling A, Martínez MJ, Martínez AT, Bergbauer M, Szewzyk U (1998) Transformation of industrial dyes by manganese peroxidases from Bjerkandera adusta and Pleurotus eryngii in a manganese-independent reaction. Appl Environ Microbiol 64:2788–2793

    PubMed  CAS  Google Scholar 

  • Itoh K, Kitade Y, Yatone C (1996) A pathway for biodegradation of anthraquinone dye, C. I. disperse red 15, by a yeast strain Pichia anomala. Bull Environ Contam Toxicol 56:413–418. doi:10.1007/s001289900059

    Article  PubMed  CAS  Google Scholar 

  • Itoh K, Kitade Y, Yatone C (1998) Oxidative biodegradation of an anthraquinone dye, pigment violet 12, by Coriolus versicolor. Bull Environ Contam Toxicol 60:786–790. doi:10.1007/s001289900695

    Article  PubMed  CAS  Google Scholar 

  • Jones P (2001) Roles of water in heme peroxidase and catalase mechanisms. J Biol Chem 276:13791–13796

    PubMed  CAS  Google Scholar 

  • Kim SJ, Shoda M (1999) Purification and characterization of a novel peroxidase from Geotricum candidum Dec 1 involved in decolorization of dyes. Appl Environ Microbiol 65:1029–1035

    PubMed  CAS  Google Scholar 

  • Kim SJ, Ishikawa K, Hirai M, Shoda M (1995) Characteristics of a newly isolated fungus, Geotrichum candidum Dec 1, which decolorizes various dyes. J Ferment Bioeng 79:601–607. doi:10.1016/0922-338X(95)94755-G

    Article  CAS  Google Scholar 

  • McMullan G, Meehan C, Conneely A, Kirby N, Robinson T, Nigam P, Banat IM, Marchant R, Smyth WF (2001) Microbial decolourisation and degradation of textile dyes. Appl Microbiol Biotechnol 56:81–87. doi:10.1007/s002530000587

    Article  PubMed  CAS  Google Scholar 

  • Ollikka P, Alhonmaki K, Leppanen VM, Glumoff T, Raijola T, Suominen I (1993) Decolorization of azotriphenyl methane, heterocyclic, and polymeric dyes by lignin peroxidase isozymes from Phanerochaete chrysosporium. Appl Environ Microbiol 59:4010–4016

    PubMed  CAS  Google Scholar 

  • Pasti MB, Crawford DL (1991) Relationship between the abilities of streptomycetes to decolorize three anthron-type dyes and to degrade lignocellulose. Can J Microbiol 37:902–907

    Article  CAS  Google Scholar 

  • Reszka KJ, Wagner BA, Burns CP, Britigan BE (2005) Effects of peroxidase substrates on the amplex red/peroxidase assay: antioxidant properties of anthracycline. Anal Biochem 342:327–337. doi:10.1016/j.ab.2005.04.017

    Article  PubMed  CAS  Google Scholar 

  • Scheibner M, Hülsdau B, Zelena K, Nimtz M, de Boer L, Berger RG, Zorn H (2008) Novel peroxidases of Marasmius acorodonius degrade β-carotene. Appl Microbiol Biotechnol 77:1241–1250. doi:10.1007/s00253-007-1261-9

    Article  PubMed  CAS  Google Scholar 

  • Stolz A (2001) Basic and applied aspects in the microbial degradation of azo dyes. Appl Microbiol Biotechnol 56:69–80. doi:10.1007/s002530100686

    Article  PubMed  CAS  Google Scholar 

  • Sturm A, Schierhorn A, Lindenstrauss U, Lilie H, Brüser T (2006) YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins. J Biol Chem 281:13972–13978. doi:10.1074/jbc.M511891200

    Article  PubMed  CAS  Google Scholar 

  • Sugano Y, Sasaki K, Shoda M (1999) cDNA cloning and genetic analysis of a novel decolorizing enzyme, peroxidase gene dyp from Geotrichum candidum Dec 1. J Biosci Bioeng 87:411–417. doi:10.1016/S1389-1723(99)80087-5

    Article  PubMed  CAS  Google Scholar 

  • Sugano Y, Nakano R, Sasaki K, Shoda M (2000) Efficient heterologous expression in Aspergillus oryzae of a unique dye-decolorizing peroxidase, DyP, of Geotrichum candidum Dec 1. Appl Environ Microbiol 66:1754–1758. doi:10.1128/AEM.66.4.1754-1758.2000

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1007/s00253-006-0545-9

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1074/jbc.M706996200

    Article  PubMed  CAS  Google Scholar 

  • Vyas BR, Molitoris HP (1995) Involvement of an extracellular H2O2-dependent ligninolytic activity of the white rot fungus Pleurotus ostreatus in the decolorization of remazol brilliant blue R. Appl Environ Microbiol 61:3919–3927

    PubMed  CAS  Google Scholar 

  • Young L, Yu J (1997) Ligninase-catalysed decolorization of synthetic dyes. Water Res 31:1187–1193. doi:10.1016/S0043-1354(96)00380-6

    Article  CAS  Google Scholar 

  • Zubieta C, Joseph R, Krishna SS, McMullan D, Kapoor M, Axelrod HL, Miller MD, Abdubek P, Acosta C, Astakhova T, other 37 authors (2007a) Identification and structural characterization of heme binding in a novel dye-decolorizing peroxidase, TyrA. Proteins 69:234–243. doi:10.1002/prot.21673

  • Zubieta C, Krishna SS, Kapoor M, Kozbial P, McMullan D, Axelrod HL, Miller MD, Abdubek P, Ambing E, Astakhova T, other 34 authors (2007b) Crystal structures of two novel dye-decolorizing peroxidases reveal a β-barrel fold with a conserved heme-binding motif. Proteins 69:223–233. doi:10.1002/prot.21550

Download references

Acknowledgments

We thank Dr. Kazutsugu Matsumoto, Meisei University, for helpful discussion on identification of reaction products, and Dr. Yoshiyuki Nakamura, Tokyo Institute of Technology, and Etsuko Suzuki, Japan Waters Co., for technical support during NMR analysis and LC-MS analysis, respectively.

Author information

Authors and Affiliations

  1. R1-30 Chemical Resources Laboratory, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama, 226-8503, Japan

    Yasushi Sugano, Yuko Matsushima, Katsunori Tsuchiya, Hirokazu Aoki, Mitsuyo Hirai & Makoto Shoda

Authors
  1. Yasushi Sugano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuko Matsushima
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katsunori Tsuchiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hirokazu Aoki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mitsuyo Hirai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Makoto Shoda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasushi Sugano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sugano, Y., Matsushima, Y., Tsuchiya, K. et al. Degradation pathway of an anthraquinone dye catalyzed by a unique peroxidase DyP from Thanatephorus cucumeris Dec 1. Biodegradation 20, 433–440 (2009). https://doi.org/10.1007/s10532-008-9234-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-008-9234-y

Keywords

Search

Navigation