Skip to main content
Log in

Manganese Peroxidases from Ganoderma applanatum Degrade β-Carotene Under Alkaline Conditions

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

A β-carotene-degrading enzyme activity was observed in liquid cultures of the basidiomycete Ganoderma applanatum. Supplementing the cultures with β-carotene induced the bleaching activity. Purification via hydrophobic interaction, ion exchange and size exclusion chromatography followed by sodium dodecyl sulphate-polyacrylamide gel electrophoresis (SDS-PAGE) resulted in a single protein band. LC-ion-trap-MS analyses and gene amplification identified two manganese peroxidase isoenzymes with 97.8 % identity on the amino acid level. These showed an estimated molecular mass of 48 kDa and an isoelectric point of 2.6. Properties not yet described for other manganese peroxidases were hydrogen-peroxide-independent catalysis and two maxima of the bleaching activity, a distinct one at pH 5 and a lower one at pH 8. During simulated washing studies, the applicability of the isoenzymes for the brightening of carotenoids under alkaline conditions was proven. The new enzymes may replace common bleaching agents to produce environmentally more compatible detergent formulations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CD-activity:

Carotene-degrading activity

HIC:

Hydrophobic interaction chromatography

SEC:

Size exclusion chromatography

MS:

Mass spectrometry

Gap:

Ganoderma applanatum

MnP:

Manganese peroxidase

References

  1. Jurado, E., Bravo, V., Luzón, G., Fernández-Serrano, M., García-Román, M., Altmajer-Vaz, D., & Vicaria, J. M. (2007). Hard-surface cleaning using lipases: enzyme-surfactant interactions and washing tests. Journal of Surfactants and Detergents, 10, 61–70.

    Article  CAS  Google Scholar 

  2. Gupta, R., Beg, Q., & Lorenz, P. (2002). Bacterial alkaline proteases: molecular approaches and industrial applications. Applied Microbiology and Biotechnology, 59, 15–32.

    Article  CAS  Google Scholar 

  3. Houde, A., Kademi, A., & Leblanc, D. (2004). Lipases and their industrial applications. Applied Biochemistry and Biotechnology, 118, 155–170.

    Article  CAS  Google Scholar 

  4. Borenstein, B., & Bunnell, R. H. (1966). Carotenoids: properties, occurrence, and utilization in foods. In C. O. Chichester, E. M. Mrak, G. F. Stewart (eds.), Advances in Food Research, vol. 15 (pp. 195–276). New York: Academic Press.

  5. Gélinas, P., Poitras, E., McKinnon, C. M., & Morin, A. (1998). Oxido-reductases and lipases as dough-bleaching agents. Cereal Chemistry, 75, 810–814.

    Article  Google Scholar 

  6. Zorn, H., Langhoff, S., Scheibner, M., & Berger, R. G. (2003). Cleavage of β, β-carotene to flavor compounds by fungi. Applied Microbiology and Biotechnology, 62, 331–336.

    Article  CAS  Google Scholar 

  7. Mendonça Maciel, M. J., Castro e Silva, A., Telles Ribeiro, H. C. (2010). Industrial and biotechnological applications of ligninolytic enzymes of the basidiomycota: a review. Electronic Journal of Biotechnology, 13(6). doi:10.2225/vol13-issue6-fulltext-2.

  8. Bibi, I., Bhatti, H. N., & Asgher, M. (2009). Decolourisation of direct dyes with manganese peroxidase from white rot basidiomycete Ganoderma lucidum-IBL-5. Canadian Journal of Chemical Engineering, 87, 435–440.

    Article  CAS  Google Scholar 

  9. Bibi, I., & Bhatti, H. (2012). Enhanced biodecolorization of reactive dyes by basidiomycetes under static conditions. Applied Biochemistry and Biotechnology, 166, 2078–2090.

    Article  CAS  Google Scholar 

  10. Ma, L., Zhuo, R., Liu, H., Yu, D., Jiang, M., Zhang, X., & Yang, Y. (2014). Efficient decolorization and detoxification of the sulfonated azo dye Reactive Orange 16 and simulated textile wastewater containing Reactive Orange 16 by the white-rot fungus Ganoderma sp. En3 isolated from the forest of Tzu-chin Mountain in China. Biochemical Engineering Journal, 82, 1–9.

    Article  CAS  Google Scholar 

  11. Scheibner, M., Hülsdau, B., Zelena, K., Nimtz, M., de Boer, L., Berger, R., & Zorn, H. (2008). Novel peroxidases of Marasmius scorodonius degrade β-carotene. Applied Microbiology and Biotechnology, 77, 1241–1250.

    Article  CAS  Google Scholar 

  12. Schüttmann, I., Bouws, H., Szweda, R. T., Suckow, M., Czermak, P., & Zorn, H. (2014). Induction, characterization, and heterologous expression of a carotenoid degrading versatile peroxidase from Pleurotus sapidus. Journal of Molecular Catalysis B: Enzymatic, 103, 79–84.

    Article  Google Scholar 

  13. Zelena, K., Hardebusch, B., Hülsdau, B., Berger, R. G., & Zorn, H. (2009). Generation of norisoprenoid flavors from carotenoids by fungal peroxidases. Journal of Agricultural and Food Chemistry, 57, 9951–9955.

    Article  CAS  Google Scholar 

  14. Zorn, H., Langhoff, S., Scheibner, M., Nimtz, M., & Berger, R. G. (2003). A peroxidase from Lepista irina cleaves β, β-carotene to flavor compounds. Biological Chemistry, 384, 1049.

    Article  CAS  Google Scholar 

  15. Grbavčić, S., Bezbradica, D., Izrael-Živković, L., Avramović, N., Milosavić, N., Karadžić, I., & Knežević-Jugović, Z. (2011). Production of lipase and protease from an indigenous pseudomonas aeruginosa strain and their evaluation as detergent additives: compatibility study with detergent ingredients and washing performance. Bioresource Technology, 102, 11226–11233.

    Article  Google Scholar 

  16. Britton, H. T. S., & Robinson, R. A. (1931). CXCVIII.-Universal buffer solutions and the dissociation constant of veronal. Journal of the Chemical Society, 1456–1462.

  17. Artimo, P., Jonnalagedda, M., Arnold, K., Baratin, D., Csardi, G., de Castro, E., Duvaud, S., Flegel, V., Fortier, A., Gasteiger, E., Grosdidier, A., Hernandez, C., Ioannidis, V., Kuznetsov, D., Liechti, R., Moretti, S., Mostaguir, K., Redaschi, N., Rossier, G., Xenarios, I., & Stockinger, H. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Research, 40, W597–W603.

    Article  CAS  Google Scholar 

  18. Altschul, S. F., Gish, W., Miller, W., Meyers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    Article  CAS  Google Scholar 

  19. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., Gonzales, N. R., Gwadz, M., Hurwitz, D. I., Jackson, J. D., Ke, Z., Lanczycki, C. J., Lu, F., Marchler, G. H., Mullokandov, M., Omelchenko, M. V., Robertson, C. L., Song, J. S., Thanki, N., Yamashita, R. A., Zhang, D., Zhang, N., Zheng, C., & Bryant, S. H. (2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Research, 39, D225–D229.

    Article  CAS  Google Scholar 

  20. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.

    Article  CAS  Google Scholar 

  21. NetNGlyc 1.0 Server 2004. Available from: http://www.cbs.dtu.dk/services/NetNGlyc/abstract.php. Accessed 2 October 2013.

  22. Steentoft, C., Vakhrushev, S. Y., Joshi, H. J., Kong, Y., Vester-Christensen, M. B., Schjoldager, K. T. B. G., Lavrsen, K., Dabelsteen, S., Pedersen, N. B., Marcos-Silva, L., Gupta, R., Paul Bennett, E., Mandel, U., Brunak, S., Wandall, H. H., Levery, S. B., & Clausen, H. (2013). Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO Journal, 32, 1478–1488.

    Article  CAS  Google Scholar 

  23. Maeda, Y., Kajiwara, S., & Ohtaguchi, K. (2001). Manganese peroxidase gene of the perennial mushroom Elfvingia applanata: cloning and evaluation of its relationship with lignin degradation. Biotechnology Letters, 23, 103–109.

    Article  CAS  Google Scholar 

  24. Nie, G., Reading, N. S., & Aust, S. D. (1999). Relative stability of recombinant versus native peroxidases from Phanerochaete chrysosporium. Archives of Biochemistry and Biophysics, 365, 328–334.

    Article  CAS  Google Scholar 

  25. Hofrichter, M. (2002). Review: lignin conversion by manganese peroxidase (MnP). Enzyme and Microbial Technology, 30, 454–466.

    Article  CAS  Google Scholar 

  26. Arnao, M. B., Acosta, M., del Río, J. A., Varón, R., & García-Cánovas, F. (1990). A kinetic study on the suicide inactivation of peroxidase by hydrogen peroxide. Biochimica et Biophysica Acta, 1041, 43–47.

    Article  CAS  Google Scholar 

  27. Wariishi, H., Akileswaran, L., & Gold, M. H. (1988). Manganese peroxidase from the basidiomycete Phanerochaete chrysosporium: spectral characterization of the oxidized states and the catalytic cycle. Biochemistry, 27, 5365–5370.

    Article  CAS  Google Scholar 

  28. Baranska, M., Schütze, W., & Schulz, H. (2006). Determination of lycopene and β-carotene content in tomato fruits and related products: comparison of FT-raman, ATR-IR, and NIR spectroscopy. Analytical Chemistry, 78, 8456–8461.

    Article  CAS  Google Scholar 

  29. Maurer, K.-H., & Flickinger, M. C. (2009). Enzymes, detergent, in encyclopedia of industrial biotechnology (Vol. 1, pp. 1–16). Weinheim: Wiley.

    Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the essential support from Henkel AG & Co. KGaA, 328 Düsseldorf, Germany. Furthermore, we wish to thank R. H. Leonhardt for his valuable assistance in molecular biology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Isabel Lanfermann.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lanfermann, I., Linke, D., Nimtz, M. et al. Manganese Peroxidases from Ganoderma applanatum Degrade β-Carotene Under Alkaline Conditions. Appl Biochem Biotechnol 175, 3800–3812 (2015). https://doi.org/10.1007/s12010-015-1548-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-015-1548-8

Keywords

Navigation