Turning points in the evolution of peroxidase-catalase superfamily: Molecular phylogeny of hybrid heme peroxidases

Cellular and Molecular Life Sciences

Volumn 71, Issue 23, 2014, Pages 4681-4696

  Zámocký, Marcel ^a,b   Gasselhuber, Bernhard ^a   Furtmüller, Paul G ^a   Obinger, Christian ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Hybrid type heme b peroxidase; Molecular evolution; Multifunctional enzymes; Peroxidase catalase superfamily; WSC domain

Indexed keywords

CATALASE; PEROXIDASE;

AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; GENETICS; HUMAN; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PHYLOGENY; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; CATALASE; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEROXIDASE; PHYLOGENY; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

EID: 84922393039     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1643-y     Document Type: Article

References (60)

1. Zamocky M, Obinger C (2010) Molecular phylogeny of heme peroxidases. In: Torres E, Ayala M (eds) Biocatalysis based on heme peroxidases. Springer, Heidelberg, pp 7-35. ISBN 978-3-642-12626-0
2. Zamocky M, Jakopitsch C, Furtmüller PG, Dunand C, Obinger C (2008) The peroxidase-cyclooxygenase superfamily: reconstructed evolution of critical enzymes of the innate immune system. Proteins 72:589-605
3. Goblirsch B, Kurker RC, Streit BR, Wilmot CM, DuBois JL (2011) Chlorite dismutases, DyPs, and EfeB: 3 microbial heme enzyme families comprise the CDE structural superfamily. J Mol Biol 408:379-398
4. Passardi F, Theiler G, Zamocky M, Cosio C, Rouhier N, Teixera F, Margis-Pinheiro M, Ioannidis V, Penel C, Falquet L, Dunand C (2007) PeroxiBase: the peroxidase database. Phytochemistry 68:1605-1611
5. Vlasits J, Jakopitsch C, Bernroitner M, Zámocký M, Furtmüller PG, Obinger C (2010) Mechanisms of catalase activity of heme peroxidases. Arch Biochem Biophys 500:74-81
6. Welinder KG (1992) Superfamily of plant, fungal, and bacterial peroxidases. Curr Opin Struct Biol 2:388-393
7. Passardi F, Bakalovic N, Teixeira FK, Margis-Pinheiro M, Penel C, Dunand C (2007) Prokaryotic origins of the non-animal peroxidase superfamily and organelle-mediated transmission to eukaryotes. Genomics 89:567-579
8. Zamocky M, Furtmüller PG, Obinger C (2010) Evolution of structure and function of Class I peroxidases. Arch Biochem Biophys 500:45-57
9. Dunford HB (2010) Peroxidases and catalases. Biochemistry, biophysics, biotechnology, and physiology, 2nd edn. John Wiley, Chichester
10. Jakopitsch C, Kolarich D, Petutschnig G, Furtmüller PG, Obinger C (2003) Distal side tryptophan, tyrosine and methionine in catalase-peroxidases are covalently linked in solution. FEBS Lett 552:135-140
11. Barrows T, Bhaskar B, Poulos TL (2004) Electrostatic control of the tryptophan radical in cytochrome c peroxidase. Biochemistry 43:8826-8834
12. Gumiero A, Murphy EJ, Metcalfe CL, Moody PCE, Raven EL (2010) An analysis of substrate binding interactions in the heme peroxidase enzymes: a structural perspective. Arch Biochem Biophys 500:13-20
13. Adak S, Pal S (2013) Ascorbate peroxidase acts as a novel determiner of redox homeostasis in Leishmania. Antiox Redox Signal 19:746-754
14. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM et al (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715-1719
15. Bödeker ITM, Nygren CMR, Taylor AFS, Olson Å, Lindahl BD (2009) ClassII peroxidase-encoding genes are present in a phylogenetically wide range of ectomycorrhizal fungi. ISME J 3:1387-1395
16. Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic family in rice and its evoluton in land plants. Phytochemistry 65:1879-1893
17. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792-1797
18. Nicholas KB, Nicholas HB (1997) Genedoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors
19. Holm L, Rösenström P (2010) Dali server: conservation mapping in 3D. Nucl Acids Res 38:W545-W549
20. Gouet P, Robert X, Courcelle E (2003) ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucl Acids Res 31:3320-3323
21. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics anlysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731-2739
22. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2:953-971
23. Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Christensen MB, Schjoldager KT, Lavrsen K, Dabelsteen S, Pedersen NB, Marcos-Silva L, Gupta R, Benett EP, Mandel U, Brunak S, Wandall HH, Levery SB, Clausen H (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J 32:1478-1488
24. Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725-738
25. Glockner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, Gade D, Beck A, Borzym K, Heitmann K, Rabus R, Schlesner H, Amann R, Reinhardt R (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100:8298-8303
26. Jakopitsch C, Regelsberger G, Furtmüller PG, Rüker F, Peschek GA, Obinger C (2001) Catalase-peroxidase from Synechocystis is capable of chlorination and bromination reactions. Biochem Biophys Res Commun 287:682-687
27. Regelsberger G, Jakopitsch C, Rüker F, Peschek GA, Obinger C (1999) Spectral and kinetic studies on the oxidation of monosubstituted phenols and anilines by recombinant Synechocystis catalase-peroxidase compound I. Biochemistry 38:10480-10488
28. Zamocky M, Gasselhuber B, Furtmüller PG, Obinger C (2012) Molecular evolution of hydrogen peroxide degraging enzymes. Arch Biochem Biophys 525:131-144
29. Zamocky M, Sekot G, Buckova M, Godocikova J, Schäffer C, Farkasovsky M, Obinger C, Polek B (2013) Intracellular targeting of ascomycetous catalase-peroxidases (KatG1s). Arch Microbiol 195:393-402
30. Jasion VS, Polanco JA, Meharenna YT, Li H, Poulos TL (2011) Crystal structure of Leishmania major peroxidase and characterization of Compound I Tryptophan radical. J Biol Chem 286:24608-24615
31. Patterson WR, Poulos TL (1995) Crystal structure of recombinant pea cytosolic ascorbate peroxidase. Biochemistry 34:4331-4341
32. Nam H, Lewis NE, Lerman JA, Lee DH, Chang RL, Kim D, Palsson BO (2012) Network context and selection in the evolution to enzyme specificity. Science 337:1101-1104
33. Jakopitsch C, Wiseman B, Vlasits J, Loewen P, Obinger C (2007) Redox intermediates in the catalase cycle of catalase-peroxidase from Synechocystis, Mycobacterium tuberculosis and Burkholderia pseudomallei. Biochemistry 46:1183-1193
34. Jakopitsch C, Auer M, Ivancich A, Rüker F, Furtmüller PG, Obinger C (2003) Total conversion of bifunctional catalase-peroxidase (KatG) to monofunctional peroxidase by exchange of a conserved distal side tyrosine. J Biol Chem 278:20185-20191
35. Regelsberger G, Jakopitsch C, Rüker F, Switala J, Loewen P, Obinger C (2001) The role of distal tryptophan in the bifunctional activity of catalase-peroxidases. Biochem Soc Trans 29:99-105
36. Poulos TL, Kraut J (1980) The stereochemistry of peroxidase catalysis. J Biol Chem 255:10322-10330
37. Jakopitsch C, Regelsberger G, Furtmüller PG, Rüker F, Peschek GA, Obinger C (2002) Engineering the proximal heme cavity of catalase-peroxidase. J Inorg Biochem 91:78-86
38. Adak S, Data AK (2005) Leishmania major encodes an unusual peroxidase that is a close homologue of plant ascorbate peroxidase: a novel role of transmembrane domain. Biochem J 390:465-474
39. Hopkins JF, Spencer DF, Laboissiere S, Neilson JAD, Eveleigh RJM, Durnford DG, Gray MW, Archibald JM (2012) Proteomics reveals plastid- and periplastid-targeted proteins in the chlorarachniophyte alga Bigelowiella natans. Genome Biol Evol 4:1391-1406
40. Ishikawa T, Tajima N, Nishikawa H, Gao J, Rapolu M, Shibata H, Sawa Y, Shigeoka S (2010) Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: its unique molecular characterization. Biochem J 426:125-134
41. Mhadmi A, Noctor G, Baker A (2012) Plant catalases: peroxisomal redox guardians. Arch Biochem Biophys 525:181-194
42. Gest N, Gautier H, Stevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? J Exp Bot 64:33-53
43. Gallie DR (2013) The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. J Exp Bot 64:433-443
44. Bernroitner M, Zamocky M, Furtmüller PG, Peschek GA, Obinger C (2009) Occurrence, phylogeny, structure and function of catalases and peroxidases in cyanobacteria. J Exp Bot 60:423-440
45. Sharp KH, Mewies M, Moody PCE, Raven EL (2003) Crystal structure of the ascorbate peroxidase-ascorbate structure. Nat Struct Mol Biol 10:303-307
46. Poulos TL (2010) Thirty years of heme peroxidase structural biology. Arch Biochem Biophys 500:3-12
47. Zamocky M, Dunand C (2006) Divergent evolutionary lines of fungal cytochrome c peroxidases belonging to the superfamily of bacterial, fungal and plant heme peroxidases. FEBS Lett 580:6655-6664
48. Erman JE, Vitello LB (2002) Yeast cytochrome c peroxidase: mechanistic studies via protein engineering. Biochim Biophys Acta 1597:193-200
49. Habetha M, Bosch TC (2005) Symbiotic Hydra express a plant-like peroxidase gene during oogenesis. J Exp Biol 208:2157-2165
50. Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nature Rev Microbiol 10:641-654
51. Guo FC, Woo PTK (2009) Selected parasitosis in cultured and wild fish. Veter Parasitol 163:207-216
52. Sundaramoorthy M, Youngs HL, Gold MH, Poulos TL (2005) High-resolution crystal structure of manganese peroxidase: substrate and inhibitor complexes. Biochemistry 44:6463-6470
53. Nigro AP, Goodin DB (2010) Reaction of N-hydroxyguanidine with the ferrous-oxy state of a heme peroxidase cavity mutant: a model for the reactions of nitric oxid synthase. Arch Biochem Biophys 500:66-73
54. Mathé C, Barre A, Jourda C, Dunand C (2010) Evolution and expression of class III peroxidases. Arch Biochem Biophys 500:58-65
55. Dunand C, Mathé C, Lazzarotto F, Margis R, Margis-Pinheiro M (2011) Ascorbate peroxidase-related is not a duplicable gene. Plant Signal Behav 6:1908-1913
56. Lazzarotto F, Teixeira FK, Rosa SB, Dunand C, Fernandes CL, de Vasconcelos Fontenele A, Silveira JAG, Verli H, Margis R, Margis-Pinheiro M (2011) Ascorbate peroxidase-related (APx-R) is a new heme-containing protein functionally associated with ascorbate peroxidase but evolutionarily divergent. New Phytol 191:234-250
57. Wolf DG, Falk R, Hacham M, Theelen B, Boekhout T, Scorzetti G, Shapiro M, Block C, Salkin IF, Polacheck I (2001) Multidrug-resistant Trichosporon asahii infection of nongranulocytopenic patients in three intensive care units. J Clin Microbiol 39:4420-4425
58. Ponting CP, Hoffman K, Bork P (1999) A latrophilin/CL-1-like GPS domain in polycystin-1. Curr Biol 9:R585-R588
59. Verna J, Lodder A, Lee K, Vagts A, Ballester R (1997) A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94:13804-13809
60. Lodder AL, Lee TK, Ballester R (1999) Characterization of the Wsc1 protein, a putative receptor in the stress response of Saccharomyces cerevisiae. Genetics 152:1487-1499