Bromoperoxidases: Their Role in the Formation of HOBr and Bromoform by Seaweeds

  • R. Wever
  • M. G. M. Tromp
  • J. W. P. M. van Schijndel
  • E. Vollenbroek
  • R. L. Olsen
  • E. Fogelqvist

Abstract

The biogenic release of halogenated volatile organics from the ocean by natural sources and the biochemical pathways which lead to the production of these substances are not well understood. In this chapter, some of the marine sources are discussed and results are presented and reviewed on the role of vanadium bromoperoxidases from seaweeds in the formation of halomethanes. Further, it will be shown that most of the predominant seaweed species from the North Atlantic, which are also present in the Arctic Ocean, contain bromoperoxidases. In contrast, in members of the Desmarestiales collected in the Weddell Sea (Antarctic) which provide the bulk of the biomass of benthic seaweeds in the Antarctic waters, no bromoperoxidase activity could be detected. The distribu;tion of seaweeds with bromoperoxidase activity is correlated with the seawater concentration of bromoform.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Barre, L.A., J.W. Bottenheim, R.C. Schnell, P.J. Crutzen, and R.A. Rasmussen. 1988. Ozone destruction and photochemical reactions at polar sunrise in the lower Arctic atmosphere. Nature 334:138–141.CrossRefGoogle Scholar
  2. 2.
    Barcelo, A.R., R. Munoz, and Sabater F. 1989. Subcellular location of basic and acidic soluble isoperoxidases in lupinus. Plant Sci. 63:31–38.CrossRefGoogle Scholar
  3. 3.
    Berg, W.W., P.D. Sperry, K.A. Rahn, and E.S. Gladney. 1983. Atmospheric bromine in the Arctic. J. Geophys. Res. 88:6719–6736.CrossRefGoogle Scholar
  4. 4.
    Berg, W.W., L.E. Heidt, W. Pollock, P.D. Sperry, and R.J. Cicerone. 1984. Brominated organic species in the Arctic atmosphere. Geophys. Res. Lett. 11: 429–432.CrossRefGoogle Scholar
  5. 5.
    Bottenheim, J.W., L.A. Barrie, E. Atlas, L.E. Heidt, H. Niki, R.A. Rasmussen, and P.B. Shepson. 1990. Depletation of lower tropospheric ozone during Arctic Spring: The Polar Sunrise experiment 1988. J. Geophys. Res. 95(D11):18555–18568.CrossRefGoogle Scholar
  6. 6.
    Burreson, J.A., R.E. Moore, and P.P. Rohler. 1976. Volatile halogen compounds in the alga Asparagopsis taxiformis rhodophyta). J. Agric. Food Chem. 24:856–-861.CrossRefGoogle Scholar
  7. 7.
    Cicerone, R.J. 1981. Halogens in the atmosphere. Rev. Geophys. Space Phys. 19:123–139.CrossRefGoogle Scholar
  8. 8.
    Cicerone, R.J., L.E. Heidt, and W.H. Pollock. 1988. Measurements of atmospheric methyl bromide and bromoform. J. Geophys. Res. 93:3745–3749.CrossRefGoogle Scholar
  9. 9.
    Class, Th., R. Kohnle, and K. Ballschmiter. 1986. Chemistry of organic traces in air VII: bromo-and bromochloromethanes in air over the Atlantic Ocean. Chemo-sphere 4:429–436.CrossRefGoogle Scholar
  10. 10.
    De Boer, E., Y. Van Kooyk, M.G.M. Tromp, H. Plat, and R. Weyer. 1986. Bromoperoxidase from Ascophyllum nodosum: A novel class of enzymes containing vanadium as a prosthetic group. Biochim. Biophys. Acta 869:48–53.CrossRefGoogle Scholar
  11. 11.
    De Boer, E., M.G.M. Tromp, H. Plat, G.E. Krenn, and R. Weyer. 1986. Vana-dium (V) as an essential element for haloperoxidase activity in marine brown algae: purification and characterization of a vanadium (V) containing bromoperoxidase from Laminaria saccharina. Biochim. Biophys. Acta 872:104–115.CrossRefGoogle Scholar
  12. 12.
    De Boer, E., and R. Weyer. 1987. Some structural and kinetic aspects of vanadium bromoperoxidases from the marine brown alga Ascophyllum nodosum. Receuil. Tray. Chim. Pays-Bas 106:409.Google Scholar
  13. 13.
    De Boer, E., and R. Weyer. 1988. The reaction mechanism of the novel vanadium bromoperoxidase: a steady-state kinetic analysis. J. Biol. Chem. 263:12326–12332.Google Scholar
  14. 14.
    De Boer, E., H. Plat, M.G.M. Tromp, M.C.R. Franssen, H.C. Van Der Plas, E.M. Meijer, H.E. Schoemaker, and R. Weyer. 1987. Vanadium-containing bromoper-oxidase, an example of an oxido-reductase with high operational stability in aqueous and organic media. Biotechnol Bioeng. 30:607–610.CrossRefGoogle Scholar
  15. 15.
    Dyrssen, D., and E. Fogelqvist. 1981. Bromoform concentrations of the Arctic Ocean in the Svalbard area. Oceanol. Acta 4:313–317.Google Scholar
  16. 16.
    Everett, R.R., J.R. Kanofsky, and A. Butler. 1990. Mechanistic investigations of the novel non-heme vanadium bromoperoxidases: evidence for singlet oxygen for-mation J. Biol. Chem. 265:4908–4914.Google Scholar
  17. 17.
    Faulkner, D.J. 1984. Marine natural products: metabolites of marine algae and herbivorious marine molluscs. Natural Prod. Repts. 1:251–280.CrossRefGoogle Scholar
  18. 18.
    Fenical, W. 1979. Molecular aspects of halogen-based biosynthesis of marine natural products. Recent Adv. Phytochem. 13:219–239.Google Scholar
  19. 19.
    Fenical, W. 1982. Natural products chemistry in the marine environment. Science 215:923–928.CrossRefGoogle Scholar
  20. 20.
    Finlayson-Pitts, B.L., F.E. Livingstone, and H.N. Berko. 1990. Ozone destruction and bromine photochemistry at ground level in the Arctic spring. Nature 343: 622–625.CrossRefGoogle Scholar
  21. 21.
    Fogelqvist, E., B. Josefsson, and C. Roos. 1982. Halocarbons as tracer substances in studies of the distribution pattern of chlorinated waters in coastal areas. Environ. Sci. Technol. 16:479–482.CrossRefGoogle Scholar
  22. 22.
    Fogelqvist, E. 1985. Carbon tetrachloride, tetrachloroethane, 1,1,1,-trichloroethane and bromoform in Arctic sea water. J. Geophys. Res. 90:9181–9193.CrossRefGoogle Scholar
  23. 23.
    Fogelqvist, E., and M. Kryssel. 1988. The antropogenic and biogenic origin of low molecular weight halocarbons in a polluted fjord, the Idefjorden. Marine Pollut. Bull. 17:378–382.CrossRefGoogle Scholar
  24. 24.
    Gschwend, P.M., J.K. MacFarlane, and K.A. Newman. 1985. Volatile halogenated organic compounds released to sea water from temperate marine macroalgae. Science 227:1033–1036.CrossRefGoogle Scholar
  25. 25.
    Gschwend, P.M., and J.K. MacFarlane. 1986. Polybromomethanes, a year round study of their release to seawater from Ascophyllum nodosum and Fucus vesiculosis. In M.L. Sohn (ed.), Organic Marine Geochemistry, ACS Symposium Series 305, American Chemical Society, Washington DC, pp. 314–322.CrossRefGoogle Scholar
  26. 26.
    Hewson, W.D., and L.P. Hager. 1980. Bromoperoxidases and halogenated lipids in marine algae. J. Phycol. 16:340–345.CrossRefGoogle Scholar
  27. 27.
    Helz, G.R., and R.Y. Hsu. 1970. Volatile chloro-and bromocarbons in coastal waters. Limnol. Oceanogr. 23:859–869.Google Scholar
  28. 28.
    Itoh, N., Y. Izumi, and H. Yamada. 1986. Characterization of nonheme type bromoperoxidase in Corallina pilulifera. J. Biol. Chem. 261:5194–5200.Google Scholar
  29. 29.
    Jaworske, D.A., and G.R. Helz. 1985. Rapid consumption of bromine oxidants in river and estuarine waters. Environ. Sci. Technol. 19:1188–1191.CrossRefGoogle Scholar
  30. 30.
    Kjellman, F.R. 1883. The algae of the Arctic Sea. Kongl. Svenska Vetenskaps Akademiens Handlingar 20:1–61. Reprinted (1971) by Otto Koeltz Antiquariat Koenigstein-Taunus, B.R.D.Google Scholar
  31. 31.
    Krenn, B.E., H. Plat, and R. Wever. 1987. The bromoperoxidase from the red alga Ceramium rubrum also contains vanadium as a prosthetic group. Biochim. Biophys. Acta 912:287–291.CrossRefGoogle Scholar
  32. 32.
    Krenn, B.E., Y. Izumi, H. Yamada, and R. Wever. 1989. A comparison of different (vanadium) bromoperoxidases: the bromoperoxidase from Corallina pilulifera is also a vanadium enzyme. Biochim. Biophys. Acta 998:63–68.CrossRefGoogle Scholar
  33. 33.
    Krenn, B.E., M.G.M. Tromp, and R. Wever. 1989. The brown alga Ascophyllum nodosum contains two different vanadium bromoperoxidases. J. Biol. Chem. 264: 19287–19292.Google Scholar
  34. 34.
    Krysell, M. 1991. Bromoform in the Nansen Basin in the Arctic Ocean. Marine Chem. 33:187–197.CrossRefGoogle Scholar
  35. 35.
    Kylin, H. 1929. Über das Vorkommen vom Jodiden, Bromiden and Jodidoxydasen bei den Meeresalgen. Hoppe Seyler’s Zeit. Physiol. Chemie 186:50–84.CrossRefGoogle Scholar
  36. 36.
    Lovelock, J.E., R.J. Maggs, and R.J. Wade. 1973. Halogenated hydrocarbons in and over the Atlantic. Nature 241:194–196.CrossRefGoogle Scholar
  37. 37.
    Lovelock, J.E. 1975. Natural halocarbons in the air and in the sea. Nature 256: 193–194.CrossRefGoogle Scholar
  38. 38.
    Lüning, K. 1990. Seaweeds: Their Environment, Biogeography, and Ecophysiology, J. Wiley and Sons, New York, pp. 193–194.Google Scholar
  39. 39.
    Manthey, J.A., and L.P. Hager. 1989. Characterization of the catalytic properties of bromoperoxidase. Biochemistry 28:3052–3057.CrossRefGoogle Scholar
  40. 40.
    Moe, R.L., and P.C. Silva. 1977. Antarctic marine flora: Uniquely devoid of kelps. Science 196:1206–1208.CrossRefGoogle Scholar
  41. 41.
    Moore, R.E. 1977. Volatile compounds from marine algae. Acc. Chem. Res. 10:40–47.CrossRefGoogle Scholar
  42. 42.
    Neidleman, S.L., and J. Geigert. 1986. Biohalogenation: Principles, Basic Roles and Applications, Ellis Horwood Ltd., Chichester.Google Scholar
  43. 43.
    Palinek, B., O.C. Zafiriou, and F.M.M. Morel. 1981. Hydrogen peroxide production by a marine phytoplankter. Limnol Oceanogr. 33:1365–1369.Google Scholar
  44. 44.
    Pallaghy, C.K., J. Minchinton, G.T. Kraft, and R. Wetherby. 1983. Presence and distribution of bromine in Thysanochladioa densa (Solieriaceae, Gigertinales), a marine red alga from the Great Barrier Reef. J. Phycol. 19:204–208.CrossRefGoogle Scholar
  45. 45.
    Pedersén, M.E.E., G. Roomans, and A. v. Hofsten. 1981. Bromine in the cuticle of Polysiphonia nigrescens: Localization and content. J. Phycol. 17:105–108.CrossRefGoogle Scholar
  46. 46.
    Penkett, S.A., B.M.R. Jones, M.J. Rycrofft, and D.A. Simons. 1985. An interhemispheric comparison of the concentrations of bromine compounds in the atmosphere. Nature 318:550–553.CrossRefGoogle Scholar
  47. 47.
    Ramanathan, V., R.J. Cicerone, H.B. Singh, and J.T. Kiehl. 1985. Trace gas trends and their potential role in climate changes. J. Geophys. Res. 90:5547–5566.CrossRefGoogle Scholar
  48. 48.
    Sakshang, E., and H.R. Skjoldal. 1989. Life at the ice edge. AMBIO 1:60–67.Google Scholar
  49. 49.
    Sauvageau, C. 1926. Zur quelques algues floridées renformant du brome a l’état libre. Bull. Stat. Arch. 23:5–23.Google Scholar
  50. 50.
    Siuda, J.F., G.R. van Blaricom, P.D. Shaw, R.D. Johnson, H. White, L.P. Hager, and R.L. Rinehart. 1975. 1-iodo-3,3—dibromo—2-heptanone, 1,1,3,3,tetrabromo2 heptanone and related compounds from the red algae Bonnemaisonia hamifera. J. Amer. Chem. Soc. 97:937–939.CrossRefGoogle Scholar
  51. 51.
    Soedjak, H.S., and A. Butler. 1990. Characterization of vanadium bromoperoxidase from Macrocystis and Fucus: Reactivity of vanadium bromoperoxidase towards acyl and alkyl peroxides and bromination of amines. Biochemistry 29:7974–7981.Google Scholar
  52. 52.
    Sturges, W.T., and L.A. Barrie. 1988. Chlorine, bromine and iodine in Arctic aerosols. Atmos. Environ. 22:1179–1194.CrossRefGoogle Scholar
  53. 53.
    Svendson, P. 1959. The algal vegetation of Spitsbergen. Norsk Polar Institutt Shifter 116:3–52.Google Scholar
  54. 54.
    Theiler, R., J.C. Cook, L.P. Hager, and J.F. Siuda. 1978. Halohydrocarbon synthesis by bromoperoxidase. Science 202:1094–1096.CrossRefGoogle Scholar
  55. 55.
    Vilter, H., K.-W. Glombitza, and A. Grawe. 1983. Peroxidases from Phaeophyceae I: extraction and detection of the peroxidases. Bot. Marine 26:331–340.Google Scholar
  56. 56.
    Vilter, H. 1984. Peroxidases from Phaeophyceae: a vanadium (V) dependent per-oxidase from Ascophyllum nodosum. Phytochemistry 23:1387–1390.CrossRefGoogle Scholar
  57. 57.
    Vilter, H. 1983. Peroxidases from Phaeophyceae IV. Fractionation and location of peroxidase isoenzymes in Ascophyllum nodosum (L.) Le Jol. Bot. Marine 26: 451–455.Google Scholar
  58. 58.
    Waaland, R.J. 1981. Commercial utilization. In C.S. Lobban and M.J. Wynne (eds.), The Biology of Seaweeds, University of California Press, Berkeley and Los Angeles, pp. 726–741.Google Scholar
  59. 59.
    Wever, R., H. Plat, and E. De Boer. 1985. Isolation procedure and some properties of the bromoperoxidase from the seaweed Ascophyllum nodosum. Biochim. Biophys. Acta 830:181–186.CrossRefGoogle Scholar
  60. 60.
    Wever, R. 1988. Ozone destruction by algae in the Arctic atmosphere. Nature 335:501.CrossRefGoogle Scholar
  61. 61.
    Wever, R., G. Olafsson, B.E. Krenn, and M.G.M. Tromp. 1988. Ozone destruction and bromoform production in the Arctic: pieces of a puzzle. Abstr. 32nd IUPAC Congress, No. 210, Stockholm, Sweden.Google Scholar
  62. 62.
    Wever, R., and B.E. Krenn. 1990. Vanadium haloperoxidases. In N.D. Chasteen (ed.), Vanadium in Biological Systems, Kluwer Academic Publishers, Amsterdam, pp. 81–97.CrossRefGoogle Scholar
  63. 63.
    Wever, R., and K. Kustin. 1990. Vanadium: A biologically relevant element. Adv. Inorg. Chem. 35:81–115.CrossRefGoogle Scholar
  64. 64.
    Wever, R., M.G.M. Tromp, B.E. Krenn, A. Marjani, and M. Van Tol. 1991. Brominating activity of the seaweed A. nodosum: Impact on the biosphere. Environ. Sci. Technol. 25:446–449.CrossRefGoogle Scholar
  65. 65.
    Wever, R. 1991. Formation of halogenated gases by natural sources. In J.E. Rogers and W.B. Whitman (eds.), Microbial Production and Consumption of Greenhouse Gases: Methane, Nitrogen Oxides, and Halomethanes, American Society for Microbiology, Washington DC, pp. 277–285.Google Scholar
  66. 66.
    Wolk, C.P. 1968. Role of bromine in the formation of refractile inclusions of the vesicle cells of the Bonnemaisoniaceae (Rhodophyta). Planta 78:371–378.CrossRefGoogle Scholar
  67. 67.
    Wuosmaa, A.M., and L.P. Hager. 1990. Methyl chloride transferase: a carbocation route for biosynthesis of halometabolites. Science 249:160–162.CrossRefGoogle Scholar
  68. 68.
    Yu, H., and J.W. Whittaker. 1989. Vanadate activation of bromoperoxidase from Corallins officinales. Biochem. Biophys. Res. Commun. 160:87–92.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1993

Authors and Affiliations

  • R. Wever
    • 1
  • M. G. M. Tromp
    • 1
  • J. W. P. M. van Schijndel
    • 1
  • E. Vollenbroek
    • 1
  • R. L. Olsen
    • 2
  • E. Fogelqvist
    • 3
  1. 1.E.C. Slater Institute for Biochemical Research and Biotechnological CentreAmsterdamThe Netherlands
  2. 2.Norwegian Institute of Fisheries and AquacultureTromsøNorway
  3. 3.Oceanographic LaboratorySwedish Meteorological and Hydrological InstituteGöteborgSweden

Personalised recommendations