JBIC Journal of Biological Inorganic Chemistry

, Volume 10, Issue 2, pp 156–166

Vanadium-dependent iodoperoxidases in Laminaria digitata, a novel biochemical function diverging from brown algal bromoperoxidases

  • Carole Colin
  • Catherine Leblanc
  • Gurvan Michel
  • Elsa Wagner
  • Emmanuelle Leize-Wagner
  • Alain Van Dorsselaer
  • Philippe Potin
Original Article

Abstract

The brown alga Laminaria digitata features a distinct vanadium-dependent iodoperoxidase (vIPO) activity, which has been purified to electrophoretic homogeneity. Steady-state analyses at pH 6.2 are reported for vIPO (KmI−=2.5 mM; kcatI−=462 s−1) and for the previously characterised vanadium-dependent bromoperoxidase in L. digitata (KmI−=18.1 mM; kcatI−=38 s−1). Although the vIPO enzyme specifically oxidises iodide, competition experiments with halides indicate that bromide is a competitive inhibitor with respect to the fixation of iodide. A full-length complementary ANA (cDNA) was cloned and shown to be actively transcribed in L. digitata and to encode the vIPO enzyme. Mass spectrometry analyses of tryptic digests of vIPO indicated the presence of at least two very similar proteins, in agreement with Southern analyses showing that vIPOs are encoded by a multigenic family in L. digitata. Phylogenetic analyses indicated that vIPO shares a close common ancestor with brown algal vanadium-dependent bromoperoxidases. Based on a three-dimensional structure model of the vIPO active site and on comparisons with those of other vanadium-dependent haloperoxidases, we propose a hypothesis to explain the evolution of strict specificity for iodide in L. digitata vIPO.

Keywords

Vanadium Haloperoxidase Iodoperoxidase Halide specificity Laminaria digitata 

Abbreviations

bp

base pair

BPO

Bromoperoxidase

cDNA

Complementary DNA

CPO

Chloroperoxidase

HPO

Haloperoxidase

IPO

Iodoperoxidase

LC

Liquid chromatography

mRNA

Messenger RNA

MS/MS

Tandem mass spectrometry

PAGE

Polyacrylamide gel electrophoresis

PCR

Polymerase chain reaction

RACE

Rapid amplification of cDNA ends

SDS

Sodium dodecyl sulphate

SSC

Saline–sodium citrate

UTR

Untranslated region

vBPO

Vanadium-dependent BPO

vCPO

Vanadium-dependent CPO

vHPO

Vanadium-dependent HPO

vIPO

Vanadium-dependent IPO

References

  1. 1.
    Gribble GW (2003) Chemosphere 52:289–297CrossRefPubMedGoogle Scholar
  2. 2.
    Littlechild JA (1999) Curr Opin Chem Biol 3:28–34Google Scholar
  3. 3.
    de Boer E, Wever R (1988) J Biol Chem 263:12326–12332Google Scholar
  4. 4.
    Arber JM, de Boer E, Garner CD, Hasnain SS, Wever R (1989) Biochemistry 28:7968–7973Google Scholar
  5. 5.
    Vilter H (1995) In: Sigel H, Sigel A (eds) Metal ions in biological systems. vol. 31 Marcel Dekker, Inc., New York, Basel, Hong Kong, pp325–362Google Scholar
  6. 6.
    Vollenbroek EGM, Simons LH, van Schijndel JW, Barnett P, Balzar M, Dekker HL, van der Linden C, Wever R (1995) Biochem Soc Trans 23:267–271Google Scholar
  7. 7.
    Barnett P, Hemrika W, Dekker HL, Muijsers AO, Renirie R, Wever R (1998) J Biol Chem 273:23381–23387Google Scholar
  8. 8.
    Plat H, Krenn BE, Wever R (1987) Biochem J 248:277–279Google Scholar
  9. 9.
    Messerschmidt A, Wever R (1996) Proc Natl Acad Sci USA 93:392–396Google Scholar
  10. 10.
    Weyand M, Hecht HJ, Kiess M, Liaud M-F, Vilter H, Schomburg D (1999) J Mol Biol 293:595–611Google Scholar
  11. 11.
    Isupov MN, Dalby AR, Brindley AA, Izumi Y, Tanabe T, Murshudov GN, Littlechild JA (2000) J Mol Biol 299:1035–1049Google Scholar
  12. 12.
    Butler A, Carter JN, Simpson MT (2001) In: Bertini I, Sigel A, Sigel H (eds) Handbook on metalloproteins. Marcel Dekker, Inc, New York, Basel uijsers AO, pp153–179Google Scholar
  13. 13.
    Tanaka N, Hasan Z, Wever R (2003) Inorg Chim Acta 356:288–296Google Scholar
  14. 14.
    Carter JN, Beatty KE, Simpson MT, Butler A (2002) J Inorg Biochem 91:59–69Google Scholar
  15. 15.
    Messerschmidt A, Prade L, Wever R (1997) Biol Chem 378:309–315Google Scholar
  16. 16.
    Hemrika W, Renirie R, Macedo-Ribeiro S, Messerschmidt A, Wever R (1999) J Biol Chem 274:23820–23827Google Scholar
  17. 17.
    Butler A (1999) Coord Chem Rev 187:17–35Google Scholar
  18. 18.
    Renirie R, Hemrika W, Wever R (2000) J Biol Chem 275:11650–11657Google Scholar
  19. 19.
    Dau H, Dittmer J, Epple M, Hanss J, Kiss E, Rehder D, Schulzke C, Vilter H (1999) FEBS Lett 457:237–240Google Scholar
  20. 20.
    Colin C, Leblanc C, Wagner E, Delage L, Leize-Wagner E, van Dorsselaer A, Kloareg B, Potin P (2003) J Biol Chem 278:23545–23552Google Scholar
  21. 21.
    Apt KE, Clendennen SK, Powers DA, Grossman AR (1995) Mol Gen Genet 246:455–464Google Scholar
  22. 22.
    Crépineau F, Roscoe T, Kaas R, Kloareg B, Boyen C (2000) Plant Mol Biol 43:503–513Google Scholar
  23. 23.
    Katoh K, Misawa K, Kuma K, Miyata T (2002) Nucleic Acids Res 30:3059–3066CrossRefGoogle Scholar
  24. 24.
    Gouet P, Robert X, Courcelle E (2003) Nucleic Acids Res 31:3320–3323Google Scholar
  25. 25.
    Fitch WM (1971) Syst Zool 20:406–416Google Scholar
  26. 26.
    Galtier N, Gouy M, Gautier C (1996) Comput Appl Biosci 12:543–548PubMedGoogle Scholar
  27. 27.
    Saitou N, Nei M (1987) Mol Biol Evol 4:406–425PubMedGoogle Scholar
  28. 28.
    Felsenstein J (1985) Evolution 39:783–791Google Scholar
  29. 29.
    Guex N, Peitsch MC (1997) Electrophoresis 18:2714–272321PubMedGoogle Scholar
  30. 30.
    Littlechild JA, Garcia-Rodriguez E, Dalby AR, Isupov MN (2002) J Mol Recognit 15:291–296Google Scholar
  31. 31.
    Bhattacharya D, Medlin L (1998) Plant Physiol 116:9–15Google Scholar
  32. 32.
    Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF (2000) Science 290:972–977CrossRefPubMedGoogle Scholar
  33. 33.
    Draisma SGA, Peters AF, Fletcher RL (2003) In: Norton TA (ed) Out of the past. The British phycological society, pp87–102Google Scholar
  34. 34.
    Almeida M, Filipe S, Humanes M, Maia MF, Melo R, Severino N, da Silva JAL, Frausto da Silva JJR, Wever R (2001) Phytochemistry 57:633–642Google Scholar
  35. 35.
    Verschueren KH, Kingma J, Rozeboom HJ, Kalk KH, Janssen DB, Dijkstra BW (1993) Biochemistry 32:9031–9037Google Scholar
  36. 36.
    Machius M, Wiegand G, Huber R (1995) J Mol Biol 246:545–559CrossRefPubMedGoogle Scholar
  37. 37.
    Fukuyama K, Sato K, Itakura H, Takahashi S, Hosoya T (1997) J Biol Chem 272:5752–5756Google Scholar
  38. 38.
    Fiedler TJ, Davey CA, Fenna RE (2000) J Biol Chem 275:11964–11971Google Scholar
  39. 39.
    Saenko GN, Kravtsova YY, Ivanenko VV, Sheludko S I (1978) Mar Biol 47:243–250Google Scholar

Copyright information

© SBIC 2005

Authors and Affiliations

  • Carole Colin
    • 1
  • Catherine Leblanc
    • 1
  • Gurvan Michel
    • 1
  • Elsa Wagner
    • 2
  • Emmanuelle Leize-Wagner
    • 2
  • Alain Van Dorsselaer
    • 2
  • Philippe Potin
    • 1
  1. 1.Station Biologique, UMR 7139 CNRSGoëmar-Université Pierre & Marie CurieRoscoff CedexFrance
  2. 2.Laboratoire de Spectrométrie de Masse Bio-Organique, UMR 7509CNRS-Université Louis PasteurStrasbourg Cedex 2France

Personalised recommendations