Skip to main content
SpringerLink
Log in

Manganese peroxidase of Agaricus bisporus: grain bran-promoted production and gene characterization

  • Biotechnologically Relevant Enzymes and Proteins
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The main manganese peroxidase (MnP) isoenzyme of Agaricus bisporus ATCC 62459 produced in lignocellulose-containing cultures was isolated, cloned and sequenced. In liquid medium, where MnP was previously detected only in trace amounts, the production of MnP was enhanced by rye and wheat bran supplements. The pI (3.25) and N-terminal amino acid sequence (25 aa) of the enzyme from bran-containing cultures were identical to those reported from compost-isolated MnP1. MnP1 is a 328-aa long polypeptide preceded by a 26-aa leader peptide. The nucleotide sequence and putative amino acid sequence of MnP1 reveal its similarity to Pleurotus ostreatus MnP3 (62.5%), Lepista irina versatile peroxidase (VP) (61.8%) and Pleurotus eryngii VPs VPL2 and VPL1 (61.9% and 61.2%, respectively). The intron-exon structure resembles that of P. ostreatus MnP1 and P. eryngii VPL1. Despite the sequence similarity to VPs, in the A. bisporus MnP1 sequence, alanine (A163) is present instead of tryptophane (W164), distinguishing it from the veratryl alcohol oxidising P. eryngii VPLs. The MnP sequence can be used as a tool to examine the pattern of ligninolytic gene expression during the growth and fruiting of A. bisporus to optimise compost composition, fungal growth and mushroom production.

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

Similar content being viewed by others

References

  • Asada Y, Watanabe A, Irie T, Nakayama T, Kuwahara M (1995) Structures of genomic and complementary DNAs coding for Pleurotus ostreatus manganese (II) peroxidase. Biochim Biophys Acta 1251:205–209

    Article  CAS  PubMed  Google Scholar 

  • Bonnen AM, Anton LH, Orth AB (1994) Lignin-degrading enzymes of the commercial button mushroom, Agaricus bisporus. Appl Environ Microbiol 60:960–965

    Google Scholar 

  • Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294–5299

    CAS  PubMed  Google Scholar 

  • Cohen R, Hadar Y, Yarden O (2001) Transcript and activity levels of different Pleurotus ostreatus peroxidases are differentially affected by Mn2+. Environ Microbiol 3:312–322

    Google Scholar 

  • Conesa A, Punt PJ, van den Hondel CA (2002) Fungal peroxidases: molecular aspects and applications. J Biotechnol 93:143–158. DOI 10.1016/S0168-1656(01)00394-7

    Article  CAS  PubMed  Google Scholar 

  • Cullen D (1997) Recent advances on the molecular genetics of ligninolytic fungi. J Biotechnol 53:273–289

    Article  CAS  PubMed  Google Scholar 

  • Durrant AJ, Wood DA, Cain RB (1991) Lignocellulose biodegradation by Agaricus bisporus during solid substrate fermentation. J Gen Microbiol 137:751–755

    Google Scholar 

  • Eggert C, Temp U, Dean JF, Eriksson KE (1996) A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett 391:144–148

    Article  CAS  PubMed  Google Scholar 

  • FAOSTAT (2004) http://apps.fao.org/default.jsp, 16 July 2004

  • Forrester IT, Grabski AC, Mishra C, Kelley BD, Strickland WN, Leatham GF, Burgess RR (1990) Characteristics and N-terminal amino acid sequence of a manganese peroxidase purified from Lentinula edodes cultures grown on a commercial wood substrate. Appl Microbiol Biotechnol 33:359–365

    CAS  PubMed  Google Scholar 

  • Hatakka A (2001) Biodegradation of lignin. In: Hofrichter M, Steinbüchel A (eds) Biopolymers. Wiley-VCH, Weinheim, pp 129–180

    Google Scholar 

  • Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30:454–466. DOI 10.1016/S0141-0229(01)00528-2

    Article  CAS  Google Scholar 

  • Kamitsuji H, Honda Y, Watanabe T, Kuwahara M (2004) Production and induction of manganese peroxidase isozymes in a white-rot fungus Pleurotus ostreatus. Appl Microbiol Biotechnol 65:287–294. DOI 10.1007/s00253-003-1543-9

    Article  CAS  PubMed  Google Scholar 

  • Lankinen VP, Bonnen AM, Anton LH, Wood DA, Kalkkinen N, Hatakka A, Thurston CF (2001) Characteristics and N-terminal amino acid sequence of manganese peroxidase from solid substrate cultures of Agaricus bisporus. Appl Microbiol Biotechnol 55:170–176. DOI 10.1007/s002530000509

    Article  CAS  PubMed  Google Scholar 

  • Li K, Xu F, Eriksson KE (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 65:2654–2660

    Google Scholar 

  • Maijala P, Harrington TC, Raudaskoski M (2003) A peroxidase gene family and gene trees in Heterobasidion and related genera. Mycologia 95:209–221

    CAS  Google Scholar 

  • Martínez AT (2002) Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzyme Microb Technol 30:425–444. DOI 10.1016/S0141-0229(01)00521-X

    Article  Google Scholar 

  • Martínez MJ, Ruiz-Duenas FJ, Guillen F, Martínez AT (1996) Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus eryngii. Eur J Biochem 237:424–432

    PubMed  Google Scholar 

  • Niku-Paavola M-L, Karhunen E, Kantelinen A, Viikari T, Lundell T, Hatakka A (1990) The effect of culture conditions on the production of lignin modifying enzymes by the white-rot fungus Phlebia radiata. J Biotechnol 13:211–221

    Article  CAS  Google Scholar 

  • Orth AB, Royse DJ, Tien M (1993) Ubiquity of lignin-degrading peroxidases among various wood-degrading fungi. Appl Environ Microbiol 59:4017–4023

    Google Scholar 

  • Pease EA, Aust SD, Tien M (1991) Heterologous expression of active manganese peroxidase from Phanerochaete chrysosporium using the baculovirus expression system. Biochem Biophys Res Commun 179:897–903

    CAS  PubMed  Google Scholar 

  • Perry CR, Smith M, Britnell CH, Wood DA, Thurston CF (1993) Identification of two laccase genes in the cultivated mushroom Agaricus bisporus. J Gen Microbiol 139:1209–1218

    Google Scholar 

  • Pickard MA, Vandertol H, Roman R, Vazquez-Duhalt R (1999) High production of ligninolytic enzymes from white rot fungi in cereal bran liquid medium. Can J Microbiol 45:627–631

    Google Scholar 

  • Rajakumar S, Gaskell J, Cullen D, Lobos S, Karahanian E, Vicuna R (1996) Lip-like genes in Phanerochaete sordida and Ceriporiopsis subvermispora, white rot fungi with no detectable lignin peroxidase activity. Appl Environ Microbiol 62:2660–2663

    Google Scholar 

  • Ruiz-Dueñas FJ, Martínez MJ, Martínez AT (1999) Molecular characterization of a novel peroxidase isolated from the ligninolytic fungus Pleurotus eryngii. Mol Microbiol 31:223–235

    Google Scholar 

  • Steffen KT, Hatakka A, Hofrichter M (2002a) Degradation of humic acids by the litter-decomposing basidiomycete Collybia dryophila. Appl Environ Microbiol 68:3442–3448. DOI 10.1128/AEM.68.7.3442-3448.2002

    Google Scholar 

  • Steffen KT, Hofrichter M, Hatakka A (2002b) Purification and characterization of manganese peroxidases from the litter-decomposing basidiomycetes Agrocybe praecox and Stropharia coronilla. Enzyme Microb Technol 30:550–555. DOI 10.1016/S0141-0229(01)00525-7

    Article  CAS  Google Scholar 

  • Stoop JMH, Mooibroek H (1999) Advances in genetic analysis and biotechnology of the cultivated button mushroom, Agaricus bisporus. Appl Microbiol Biotechnol 52:474–483. DOI 10.1007/s002530051548

    Article  CAS  Google Scholar 

  • Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26

    Google Scholar 

  • Wariishi H, Valli K, Gold M (1992) Manganese (II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. J Biol Chem 267:23688–23695

    CAS  PubMed  Google Scholar 

  • Wood DA (1980) Production, purification and properties of extracellular laccase of Agaricus bisporus. J Gen Microbiol 117:327–338

    Google Scholar 

  • Zorn H, Langhoff S, Scheibner M, Nimtz M, Berger RG (2003) A peroxidase from Lepista irina cleaves beta,beta-carotene to flavor compounds. Biol Chem 384:1049–1056

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work was funded by the grant (#53305) from the Academy of Finland to the Center of Excellence “Microbial Resources” and a graduate school position from the University of Helsinki to P.L.

Author information

Authors and Affiliations

  1. Department of Applied Chemistry and Microbiology, Viikki, Biocenter 1, University of Helsinki, P.O. Box 56, 00014, Helsinki, Finland

    Pauliina Lankinen, Kristiina Hildén, Mirja Salkinoja-Salonen & Annele Hatakka

  2. VTT Biotechnology, P.O. Box 1500, 02044 VTT, Espoo, Finland

    Nina Aro

Authors
  1. Pauliina Lankinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristiina Hildén
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nina Aro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mirja Salkinoja-Salonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Annele Hatakka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pauliina Lankinen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lankinen, P., Hildén, K., Aro, N. et al. Manganese peroxidase of Agaricus bisporus: grain bran-promoted production and gene characterization. Appl Microbiol Biotechnol 66, 401–407 (2005). https://doi.org/10.1007/s00253-004-1731-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-004-1731-2

Keywords

Search

Navigation