Nothing Special   »   [go: up one dir, main page]
Skip to main content

Advertisement

Springer Nature Link
Log in

Molecular Evolution and Diversity of Lignin Degrading Heme Peroxidases in the Agaricomycetes

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The plant and microbial peroxidase superfamily encompasses three classes of related protein families. Class I includes intracellular peroxidases of prokaryotic origin, class II includes secretory fungal peroxidases, including the lignin degrading enzymes manganese peroxidase (MnP), lignin peroxidase (LiP), and versatile peroxidase (VP), and class III includes the secretory plant peroxidases. Here, we present phylogenetic analyses using maximum parsimony and Bayesian methods that address the origin and diversification of class II peroxidases. Higher-level analyses used published full-length sequences from all members of the plant and microbial peroxidase superfamily, while lower-level analyses used class II sequences only, including 43 new sequences generated from Agaricomycetes (mushroom-forming fungi and relatives). The distribution of confirmed and proposed catalytic sites for manganese and aromatic compounds in class II peroxidases, including residues supposedly involved in three different long range electron transfer pathways, was interpreted in the context of phylogenies from the lower-level analyses. The higher-level analyses suggest that class II sequences constitute a monophyletic gene family within the plant and microbial peroxidase superfamily, and that they have diversified extensively in the basidiomycetes. Peroxidases of unknown function from the ascomycete Magnaporthe grisea were found to be the closest relatives of class II sequences and were selected to root class II sequences in the lower-level analyses. LiPs evidently arose only once in the Polyporales, which harbors many white-rot taxa, whereas MnPs and VPs are more widespread and may have multiple origins. Our study includes the first reports of partial sequences for MnPs in the Hymenochaetales and Corticiales.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Ambert-Balay K, Fuchs SM, Tien M (1998) Identification of the veratryl alcohol binding site in lignin peroxidase by site-directed mutagenesis. Biochem Biophys Res Commun 251:283–286

    Article  PubMed  CAS  Google Scholar 

  • Banci L, Bertini I, Pease EA, Tien M, Turano P (1992) 1H NMR investigation of manganese peroxidase from Phanerochaete chrysosporium. A comparison with other peroxidases. Biochemistry 31:10009–10017

    Article  PubMed  CAS  Google Scholar 

  • Banci L, Camarero S, Martinez AT, Martinez MJ, Perez-Boada M, Pierattelli R, Ruiz-Duenas FJ (2003) NMR study of manganese(II) binding by a new versatile peroxidase from the white-rot fungus Pleurotus eryngii. J Biol Inorg Chem 8:751–760

    Article  PubMed  CAS  Google Scholar 

  • Bekker A, Holland HD, Wang PL, Rumble D 3rd, Stein HJ, Hannah JL, Coetzee LL, Beukes NJ (2004) Dating the rise of atmospheric oxygen. Nature 427:117–120

    Article  PubMed  CAS  Google Scholar 

  • Binder M, Hibbett DS, Larsson K-H, Larsson E, Langer E, Langer G (2005) The phylogenetic distribution of resupinate forms across the major clades of mushroom-forming fungi (Homobasidiomycetes). Syst Biodivers 3:113–157

    Article  Google Scholar 

  • Blodig W, Smith AT, Doyle WA, Piontek K (2001) Crystal structures of pristine and oxidatively processed lignin peroxidase expressed in Escherichia coli and of the W171F variant that eliminates the redox active tryptophan 171. Implications for the reaction mechanism. J Mol Biol 305:851–861

    Article  PubMed  CAS  Google Scholar 

  • Camarero S, Sarkar S, Ruiz-Dueñas FJ, Martínez MJ, Martínez AT (1999) Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J Biol Chem 274:10324–10330

    Article  PubMed  CAS  Google Scholar 

  • Camarero S, Ruiz-Dueñas FJ, Sarkar S, Martínez MJ, Martínez AT (2000) The cloning of a new peroxidase found in lignocellulose cultures of Pleurotus eryngii and sequence comparison with other fungal peroxidases. FEMS Microbiol Lett 191:37–43

    Article  PubMed  CAS  Google Scholar 

  • Choinowski T, Blodig W, Winterhalter KH, Piontek K (1999) The crystal structure of lignin peroxidase at 1.70 A resolution reveals a hydroxy group on the cbeta of tryptophan 171: a novel radical site formed during the redox cycle. J Mol Biol 286:809–827

    Article  PubMed  CAS  Google Scholar 

  • Doyle WA, Blodig W, Veitch NC, Piontek K, Smith AT (1998) Two substrate interaction sites in lignin peroxidase revealed by site-directed mutagenesis. Biochemistry 37:15097–15105

    Article  PubMed  CAS  Google Scholar 

  • Dunford HB (1999) Heme peroxidases. John Wiley & Sons, New York

    Google Scholar 

  • Duroux L, Welinder KG (2003) The peroxidase gene family in plants: a phylogenetic overview. J Mol Evol 57:397–407

    Article  PubMed  CAS  Google Scholar 

  • Edwards SL, Raag R, Wariishi H, Gold MH, Poulos TL (1993) Crystal structure of lignin peroxidase. Proc Natl Acad Sci USA 90:750–754

    Article  PubMed  CAS  Google Scholar 

  • Gilbertson RL (1980) Wood-rotting fungi of North America. Mycologia 72:1–49

    Article  Google Scholar 

  • Glenn JK, Morgan MA, Mayfield MB, Kuwahara M, Gold MH (1983) An extracellular H2O2-requiring enzyme preparation involved in lignin biodegradation by the white rot basidiomycete Phanerochaete chrysosporium. Biochem Biophys Res Commun 114:1077–1083

    PubMed  CAS  Google Scholar 

  • Heinfling A, Martínez MJ, Martínez AT, Bergbauer M, Szewzyk U (1998) Purification and characterization of peroxidases from the dye-decolorizing fungus Bjerkandera adusta. FEMS Microbiol Lett 165:43–50

    Article  PubMed  CAS  Google Scholar 

  • Hibbett DS (2006) A phylogenetic overview of the Agaricomycotina. Mycologia 98:917–925

    Article  PubMed  Google Scholar 

  • Hibbett DS, Donoghue MJ (2001) Analysis of character correlations among wood decay mechanisms, mating systems, and substrate ranges in homobasidiomycetes. Syst Biol 50:215–242

    Article  PubMed  CAS  Google Scholar 

  • Hibbett DS, Thorn RG (2001) Basidiomycota: Homobasidiomycetes. In: McLaughlin D, McLaughlin EG, Lemke PA (eds) The Mycota. Springer-Verlag, New York, pp 121–168

    Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, et al (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547

    Article  PubMed  Google Scholar 

  • Hildén K, Martínez AT, Hatakka A, Lundell T (2005) The two manganese peroxidases Pr-MnP2 and Pr-MnP3 of Phlebia radiata, a lignin-degrading basidiomycete, are phylogenetically and structurally divergent. Fungal Genet Biol 42:403–419

    Article  PubMed  CAS  Google Scholar 

  • Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30:454–466

    Article  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Irie T, Honda Y, Ha H-C, Watanabe T, Kuwahara M (2000) Isolation of cDNA and genomic fragments encoding the major manganese peroxidase isozyme from the white rot basidiomycete Pleurotus ostreatus. J Wood Sci 46:230–233

    Article  CAS  Google Scholar 

  • Johansson T, Nyman PO (1996) A cluster of genes encoding major isozymes of lignin peroxidase and manganese peroxidase from the white-rot fungus Trametes versicolor. Gene 170:31–38

    Article  PubMed  CAS  Google Scholar 

  • Johjima T, Itoh N, Kabuto M, Tokimura F, Nakagawa T, Wariishi H, Tanaka H (1999) Direct interaction of lignin and lignin peroxidase from Phanerochaete chrysosporium. Proc Natl Acad Sci USA 96:1989–1994

    Article  PubMed  CAS  Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41:465–505

    Article  PubMed  CAS  Google Scholar 

  • Kishi K, Kusters-van Someren M, Mayfield MB, Sun J, Loehr TM, Gold MH (1996) Characterization of manganese(II) binding site mutants of manganese peroxidase. Biochemistry 35:8986–8994

    Article  PubMed  CAS  Google Scholar 

  • Kuwahara M, Glenn JK, Morgan MA, Gold MH (1984) Separation and characterization of two extracellular H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett 169:247–250

    Article  CAS  Google Scholar 

  • Larsson KH, Larsson E, Koljalg U (2004) High phylogenetic diversity among corticioid homobasidiomycetes. Mycol Res 108:983–1002

    Article  PubMed  CAS  Google Scholar 

  • Lewis NG, Razal RA, Yamamoto E (1987) Lignin degradation by peroxidase in organic media: A reassessment. Proc Natl Acad Sci USA 84:7925–7927

    Article  PubMed  CAS  Google Scholar 

  • Maddison DR, Maddison WP (2002) MacClade4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA

    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

    Article  CAS  Google Scholar 

  • Martínez AT (2002) Molecular biology and structure-function of lignin-degrading heme peroxidases. Enzyme Microb Technol 30:425–444

    Article  Google Scholar 

  • Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695–700

    Article  PubMed  CAS  Google Scholar 

  • Matheny PB, Wang Z, Binder M, et al. (2007) Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Mol Phylogenet Evol 43:430–451

    Article  PubMed  CAS  Google Scholar 

  • Moreira PR, Duez C, Dehareng D, Antunes A, Almeida-Vara E, Frere JM, Malcata FX, Duarte JC (2005) Molecular characterisation of a versatile peroxidase from a Bjerkandera strain. J Biotechnol 118:339–352

    Article  PubMed  CAS  Google Scholar 

  • Nilsson T (1988) Defining fungal decay types—final proposal. IRG/WP/1355. International Research Group on Wood Preservation, Stockholm, Sweden

    Google Scholar 

  • Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65:1879–1893

    Article  PubMed  CAS  Google Scholar 

  • Paszczynski A, Huynh V-B, Crawford R (1985) Enzymatic activities of an extracellular, manganese-dependent peroxidase from Phanerochaete chrysosporium. Arch Biochem Biophys 242:329–341

    Article  Google Scholar 

  • Pérez-Boada M, Ruiz-Dueñas FJ, Pogni R, Basosi R, Choinowski T, Martínez MJ, Piontek K, Martínez AT (2005) Versatile peroxidase oxidation of high redox potential aromatic compounds: site-directed mutagenesis, spectroscopic and crystallographic investigation of three long-range electron transfer pathways. J Mol Biol 354:385–402

    Article  PubMed  CAS  Google Scholar 

  • Perie FH, Sheng D, Gold MH (1996) Purification and characterization of two manganese peroxidase isozymes from the white-rot basidiomycete Dichomitus squalens. Biochim Biophys Acta 1297:139–148

    PubMed  Google Scholar 

  • Pointing SB, Pelling AL, Smith GJ, Hyde KD, Reddy CA (2005) Screening of basidiomycetes and xylariaceous fungi for lignin peroxidase and laccase gene-specific sequences. Mycol Res 109:115–124

    Article  PubMed  CAS  Google Scholar 

  • Rayner ADM, Boddy L (1988) Fungal decomposition of wood, its biology and ecology. John Wiley & Sons, Chichester, UK

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  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

    Article  PubMed  Google Scholar 

  • Rüttimann-Johnson C, Cullen D, Lamar RT (1994) Manganese peroxidases of the white rot fungus Phanerochaete sordida. Appl Environ Microbiol 60:599–605

    PubMed  Google Scholar 

  • Sarkanen S, Razal RA, Piccariello T, Yamamoto E, Lewis NG (1991) Lignin peroxidase: toward a clarification of its role in vivo. J Biol Chem 266:3636–3643

    PubMed  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  PubMed  CAS  Google Scholar 

  • Schoemaker HE, Lundell TK, Floris R, Glumoff T, Winterhalter KH, Piontek K (1994) Do carbohydrates play a role in the lignin peroxidase cycle? Redox catalysis in the endergonic region of the driving force. Bioorg Med Chem 2:509–519

    Article  PubMed  CAS  Google Scholar 

  • Schwarze FWMR, Engels J, Mattheck C (2000) Fungal strategies of wood decay in trees. Springer, New York

    Google Scholar 

  • Sollewijn Gelpke MD, Lee J, Gold MH (2002) Lignin peroxidase oxidation of veratryl alcohol: effects of the mutants H82A, Q222A, W171A, and F267L. Biochemistry 41:3498–3506

    Article  PubMed  CAS  Google Scholar 

  • Sundaramoorthy M, Kishi K, Gold MH, Poulos TL (1994a) Preliminary crystallographic analysis of manganese peroxidase from Phanerochaete chrysosporium. J Mol Biol 238:845–848

    Article  PubMed  CAS  Google Scholar 

  • Sundaramoorthy M, Kishi K, Gold MH, Poulos TL (1994b) The crystal structure of manganese peroxidase from Phanerochaete chrysosporium at 2.06-A resolution. J Biol Chem 269:32759–32767

    PubMed  CAS  Google Scholar 

  • Sundaramoorthy M, Kishi K, Gold MH, Poulos TL (1997) Crystal structures of substrate binding site mutants of manganese peroxidase. J Biol Chem 272:17574–17580

    Article  PubMed  CAS  Google Scholar 

  • Sundaramoorthy M, Youngs HL, Gold MH, Poulos TL (2005) High-resolution crystal structure of manganese peroxidase: substrate and inhibitor complexes. Biochemistry 44:6463–6470

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (and other methods) 4.0 Beta. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Teixeira FK, Menezes-Benavente L, Margis R, Margis-Pinheiro M (2004) Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: inferences from the rice genome. J Mol Evol 59:761–770

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tien M, Kirk K (1983) Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium. Science 221:661–663

    Article  PubMed  CAS  Google Scholar 

  • Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–138

    Article  PubMed  CAS  Google Scholar 

  • Ward G, Hadar Y, Bilkis I, Dosoretz CG (2003) Mechanistic features of lignin peroxidase-catalyzed oxidation of substituted phenols and 1,2-dimethoxyarenes. J Biol Chem 278:39726–39734

    Article  PubMed  CAS  Google Scholar 

  • Welinder KG (1992) Superfamily of plant, fungal and bacterial peroxidases. Curr Opin Struct Biol 2:388–393

    Article  CAS  Google Scholar 

  • Welinder KG, Gajhede M (1993) Structure and evolution of peroxidases. In: Greppin H, Rasmussen SK, Welinder KG, Penel C (eds) Plant peroxidases: biochemistry and physiology. University of Copenhagen and University of Geneva, Geneva, pp 35–42

    Google Scholar 

  • Welinder KG, Justesen AF, Kjaersgard IV, Jensen RB, Rasmussen SK, Jespersen HM, Duroux L (2002) Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana. Eur J Biochem 269:6063–6081

    Article  PubMed  CAS  Google Scholar 

  • Zamocky M (2004) Phylogenetic relationships in class I of the superfamily of bacterial, fungal, and plant peroxidases. Eur J Biochem 271:3297–3309

    Article  PubMed  CAS  Google Scholar 

  • Zamocky M, Janecek S, Koller F (2000) Common phylogeny of catalase-peroxidases and ascorbate peroxidases. Gene 256:169–182

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Michael Fischer for providing the Fomitiporia mediterranea culture. We thankfully acknowledge the technical support of and helpful discussions with Manfred Binder, Brandon Matheny, Jason Slot, and Zheng Wang. We wish to thank Lisa Bukovnik for carrying out much of the sequencing at Duke University. Dan Cullen critically read the manuscript and gave helpful input, which we gratefully acknowledge.

Author information

Authors and Affiliations

  1. Department of Biology, Clark University, 950 Main Street, Worcester, MA, 01610, USA

    Ingo Morgenstern, Shlomit Klopman & David S. Hibbett

Authors
  1. Ingo Morgenstern
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shlomit Klopman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David S. Hibbett
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ingo Morgenstern.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morgenstern, I., Klopman, S. & Hibbett, D.S. Molecular Evolution and Diversity of Lignin Degrading Heme Peroxidases in the Agaricomycetes. J Mol Evol 66, 243–257 (2008). https://doi.org/10.1007/s00239-008-9079-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9079-3

Keywords

Search

Navigation