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Environmental Control of Vanadium Haloperoxidases and Halocarbon Emissions in Macroalgae

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Abstract

Vanadium-dependent haloperoxidases (V-HPO), able to catalyze the reaction of halide ions (Cl−, Br−, I-) with hydrogen peroxide, have a great influence on the production of halocarbons, which in turn are involved in atmospheric ozone destruction and global warming. The production of these haloperoxidases in macroalgae is influenced by changes in the surrounding environment. The first reported vanadium bromoperoxidase was discovered 40 years ago in the brown alga Ascophyllum nodosum. Since that discovery, more studies have been conducted on the structure and mechanism of the enzyme, mainly focused on three types of V-HPO, the chloro- and bromoperoxidases and, more recently, the iodoperoxidase. Since aspects of environmental regulation of haloperoxidases are less well known, the present paper will focus on reviewing the factors which influence the production of these enzymes in macroalgae, particularly their interactions with reactive oxygen species (ROS).

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References

  • Aguilera J, Bischof K, Karsten U, Hanelt D, Wiencke C (2002) Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress. Mar Biol 140(6):1087–1095

    Article  CAS  Google Scholar 

  • Ahern TJ, Allan GG, Medcalf DG (1980) New bromoperoxidase of marine origin. Partial purification and characterization. Biochim Biophys Acta 616(2):329–339

    Article  PubMed  CAS  Google Scholar 

  • Allen RC (1999) Method for selectively inhibiting the growth of microbes using a haloperoxidase-halide-peroxide system: Google Patents.

  • Almeida M, Humanes M, Melo R, Silva J, da Silva JF, Vilter H, Wever R (1998) Saccorhiza polyschides (Phaeophyceae; Phyllariaceae) a new source for vanadium-dependent haloperoxidases. Phytochemistry 48(2):229–239

    Article  CAS  Google Scholar 

  • Almeida MG, Humanes M, Melo R, Silva JA, da Silva JJ, Wever R (2000) Purification and characterisation of vanadium haloperoxidases from the brown alga Pelvetia canaliculata. Phytochemistry 54(1):5–11

    Article  PubMed  CAS  Google Scholar 

  • Almeida M, Filipe S, Humanes M, Maia MF, Melo R, Severino N et al (2001) Vanadium haloperoxidases from brown algae of the Laminariaceae family. Phytochemistry 57(5):633–642

    Article  PubMed  CAS  Google Scholar 

  • Amachi S, Kamagata Y, Kanagawa T, Muramatsu Y (2006) Bacteria mediate methylation of iodine in marine and terrestrial environments. Appl Environ Microbiol 67:2718–2722

    Article  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Ar Gall E, Cornec L, Deslandes E (2008) Oligocarrageenans and tissue-dependent oxidative burst in Solieria chordalis (Rhodophyceae, Gigartinales). Phycol Res 56(1):7–11

    Article  CAS  Google Scholar 

  • Aravind P, Prasad MNV (2005) Modulation of cadmium-induced oxidative stress in Ceratophyllum demersum by zinc involves ascorbate–glutathione cycle and glutathione metabolism. Plant Physiol Biochem 43(2):107–116

    Article  PubMed  CAS  Google Scholar 

  • Arizumi H, Hata K, Shimizu N (1994) Isolation and determination of structure of antioxidant chromanol derivative from Ascophyllum nodosum. Jpn Kokkai Tokyo Koho 122:160312

    Google Scholar 

  • Baden DG, Corbett MD (1980) Bromoperoxidases from Penicillus capitatus, Penicillus lamourouxii and Rhipocephalus phoenix. Biochem J 187(1):205–211

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baharum H, Chu W-C, Teo S-S, Ng K-Y, Rahim RA, Ho C-L (2013) Molecular cloning, homology modeling and site-directed mutagenesis of vanadium-dependent bromoperoxidase (GcVBPO1) from Gracilaria changii (Rhodophyta). Phytochemistry 92:49–59

    Article  PubMed  CAS  Google Scholar 

  • Baker JM, Sturges WT, Sugier J, Sunnenberg G, Lovett AA, Reeves CE et al (2001) Emissions of CH3Br, organochlorines, and organoiodines from temperate macroalgae. Chemosphere Global Change Sci 3(1):93–106

    Article  CAS  Google Scholar 

  • Bartsch I, Wiencke C, Bischof K, Buchholz CM, Buck BH, Eggert A et al (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43(1):1–86

    Article  Google Scholar 

  • Beissner RS, Guilford WJ, Coates RM, Hager LP (1981) Synthesis of brominated heptanones and bromoform by a bromoperoxidase of marine origin. Biochemistry 20(13):3724–3731

    Article  PubMed  CAS  Google Scholar 

  • Bernhardt P, Okino T, Winter JM, Miyanaga A, Moore BS (2011) A stereoselective vanadium-dependent chloroperoxidase in bacterial antibiotic biosynthesis. J Am Chem Soc 133(12):4268–4270

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bischof K, Rautenberger R (2012) Seaweed responses to environmental stress: reactive oxygen and antioxidative strategies. In: Wiencke C, Bischof K (eds) Seaweed biology, vol 219. Springer, Berlin, pp 109–132

    Chapter  Google Scholar 

  • Bischof K, Steinhoff FS (2012) Impacts of ozone stratospheric depletion and solar UVB radiation on seaweeds. Seaweed biology, vol 219. Springer, Heidelberg, pp 433–448

  • Bitton R, Ben-Yehuda M, Davidovich M, Balazs Y, Potin P, Delage L et al (2006) Structure of algal-born phenolic polymeric adhesives. Macromol Biosci 6(9):737–746

    Article  PubMed  CAS  Google Scholar 

  • Blasiak LC, Drennan CL (2009) Structural perspective on enzymatic halogenation. Acc Chem Res 42(1):147

    Article  PubMed  CAS  Google Scholar 

  • Borchardt S, Allain E, Michels J, Stearns G, Kelly R, McCoy W (2001) Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl Environ Microbiol 67(7):3174–3179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bouarab K, Potin P, Correa J, Kloareg B (1999) Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell 11(9):1635–1650

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bouarab K, Adas F, Gaquerel E, Kloareg B, Salaün J-P, Potin P (2004) The innate immunity of a marine red alga involves oxylipins from both the eicosanoid and octadecanoid pathways. Plant Physiol 135(3):1838–1848

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burreson B, Moore RE, Roller P (1975) Haloforms in the essential oil of the alga Asparagopsis taxiformis (Rhodophyta). Tetrahedron Lett 16(7):473–476

    Article  Google Scholar 

  • Butler A (1998) Vanadium haloperoxidases. Curr Opin Chem Biol 2(2):279–285

    Article  PubMed  CAS  Google Scholar 

  • Butler A (1999) Mechanistic considerations of the vanadium haloperoxidases. Coord Chem Rev 187(1):17–35

    Article  CAS  Google Scholar 

  • Butler A, Carter-Franklin JN (2004) The role of vanadium bromoperoxidase in the biosynthesis of halogenated marine natural products. Nat Prod Rep 21(1):180–188

    Article  PubMed  CAS  Google Scholar 

  • Butler A, Sandy M (2009) Mechanistic considerations of halogenating enzymes. Nature 460(7257):848–854

    Article  PubMed  CAS  Google Scholar 

  • Butler A, Walker J (1993) Marine haloperoxidases. Chem Rev 93(5):1937–1944

    Article  CAS  Google Scholar 

  • Carpenter LJ (2003) Iodine in the marine boundary layer. Chem Rev 103(12):4953–4962

    Article  PubMed  CAS  Google Scholar 

  • Carpenter LJ, Liss PS (2000) On temperate sources of bromoform and other reactive organic bromine gases. J Geophys Res Atmos 105(D16):20539–20547

    Article  CAS  Google Scholar 

  • Carpenter L, Sturges W, Penkett S, Liss P, Alicke B, Hebestreit K, Platt U (1999) Short-lived alkyl iodides and bromides at Mace Head, Ireland: links to biogenic sources and halogen oxide production. J Geophys Res Atmos 104(D1):1679–1689

    Article  CAS  Google Scholar 

  • Carpenter L, Malin G, Liss P, Küpper F (2000) Novel biogenic iodine-containing trihalomethanes and other short-lived halocarbons in the coastal east Atlantic. Glob Biogeochem Cycles 14(4):1191–1204

    Article  CAS  Google Scholar 

  • Carter JN, Beatty KE, Simpson MT, Butler A (2002) Reactivity of recombinant and mutant vanadium bromoperoxidase from the red alga Corallina officinalis. J Inorg Biochem 91(1):59–69

    Article  PubMed  CAS  Google Scholar 

  • Carter-Franklin JN, Butler A (2004) Vanadium bromoperoxidase-catalyzed biosynthesis of halogenated marine natural products. J Am Chem Soc 126(46):15060–15066

    Article  PubMed  CAS  Google Scholar 

  • Chance R, Baker AR, Küpper FC, Hughes C, Kloareg B, Malin G (2009) Release and transformations of inorganic iodine by marine macroalgae. Estuar Coast Shelf Sci 82(3):406–414

    Article  CAS  Google Scholar 

  • Christmann U, Dau H, Haumann M, Kiss E, Liebisch P, Rehder D, et al (2004) Substrate binding to vanadate-dependent bromoperoxidase from Ascophyllum nodosum: a vanadium K-edge XAS approach. Dalton Trans 16:2534–2540

  • Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621

    Article  PubMed  CAS  Google Scholar 

  • Colin C, Leblanc C, Wagner E, Delage L, Leize-Wagner E, Van Dorsselaer A et al (2003) The brown algal kelp Laminaria digitata features distinct bromoperoxidase and iodoperoxidase activities. J Biol Chem 278(26):23545–23552

    Article  PubMed  CAS  Google Scholar 

  • Colin C, Leblanc C, Michel G, Wagner E, Leize-Wagner E, Van Dorsselaer A, Potin P (2005) Vanadium-dependent iodoperoxidases in Laminaria digitata, a novel biochemical function diverging from brown algal bromoperoxidases. JBIC J Biol Inorg Chem 10(2):156–166

    Article  PubMed  CAS  Google Scholar 

  • Collén J, Davison I (1999a) Stress tolerance and reactive oxygen metabolism in the intertidal red seaweeds Mastocarpus stellatus and Chondrus crispus. Plant Cell Environ 22(9):1143–1151

    Article  Google Scholar 

  • Collén J, Davison IR (1999b) Reactive oxygen production and damage in intertidal Fucus spp. (Phaeophyceae). J Phycol 35(1):54–61

    Article  Google Scholar 

  • Collén J, Davison IR (2001) Seasonality and thermal acclimation of reactive oxygen metabolism in Fucus vesiculosus (Phaeophyceae). J Phycol 37(4):474–481

    Article  Google Scholar 

  • Collén J, Pedersén M (1996) Production, scavenging and toxicity of hydrogen peroxide in the green seaweed Ulva rigida. Eur J Phycol 31(3):265–271

    Article  Google Scholar 

  • Collén J, Del Rio MJ, García-Reina G, Pedersén M (1995) Photosynthetic production of hydrogen peroxide by Ulva rigida C. Ag. (Chlorophyta). Planta 196(2):225–230

    Article  Google Scholar 

  • Contreras L, Mella D, Moenne A, Correa JA (2009) Differential responses to copper-induced oxidative stress in the marine macroalgae Lessonia nigrescens and Scytosiphon lomentaria (Phaeophyceae). Aquat Toxicol 94(2):94–102

    Article  PubMed  CAS  Google Scholar 

  • Cosse A, Potin P, Leblanc C (2009) Patterns of gene expression induced by oligoguluronates reveal conserved and environment-specific molecular defense responses in the brown alga Laminaria digitata. New Phytol 182(1):239–250

    Article  PubMed  CAS  Google Scholar 

  • Coupe E, Smyth M, Fosberry A, Hall R, Littlechild J (2007) The dodecameric vanadium-dependent haloperoxidase from the marine algae Corallina officinalis: cloning, expression, and refolding of the recombinant enzyme. Protein Expr Purif 52(2):265–272

    Article  PubMed  CAS  Google Scholar 

  • Crans DC, Smee JJ, Gaidamauskas E, Yang L (2004) The chemistry and biochemistry of vanadium and the biological activities exerted by vanadium compounds. Chem Rev 104(2):849–902

    Article  PubMed  CAS  Google Scholar 

  • Crépineau F, Roscoe T, Kaas R, Kloareg B, Boyen C (2000) Characterisation of complementary DNAs from the expressed sequence tag analysis of life cycle stages of Laminaria digitata (Phaeophyceae). Plant Mol Biol 43(4):503–513

    Article  PubMed  Google Scholar 

  • Crockford SJ (2009) Evolutionary roots of iodine and thyroid hormones in cell–cell signaling. Integr Comp Biol 49:155–166 icp053

  • De Boer E, Tromp M, Plat H, Krenn G, Wever R (1986) Vanadium (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 Protein Struct Mol Enzymol 872(1):104–115

    Article  Google Scholar 

  • De la Coba F, Aguilera J, Figueroa F, De Gálvez M, Herrera E (2009) Antioxidant activity of mycosporine-like amino acids isolated from three red macroalgae and one marine lichen. J Appl Phycol 21(2):161–169

    Article  CAS  Google Scholar 

  • Dring MJ (2005) Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism. Adv Bot Res 43:175–207

  • Dummermuth A, Karsten U, Fisch K, König G, Wiencke C (2003) Responses of marine macroalgae to hydrogen-peroxide stress. J Exp Mar Biol Ecol 289(1):103–121

    Article  CAS  Google Scholar 

  • Dunford HB (2010) Peroxidases and catalases: biochemistry, biophysics, biotechnology and physiology. Wiley, Hoboken

    Google Scholar 

  • Everett RR, Kanofsky J, Butler A (1990) Mechanistic investigations of the novel non-heme vanadium bromoperoxidases. Evidence for singlet oxygen production. J Biol Chem 265(9):4908–4914

    PubMed  CAS  Google Scholar 

  • Fenical W (1975) Halogenation in the Rhodophyta. A review. J Phycol 11(3):245–259

    CAS  Google Scholar 

  • Fujimori DG, Walsh CT (2007) What’s new in enzymatic halogenations. Curr Opin Chem Biol 11(5):553–560

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gall EA, Küpper FC, Kloareg B (2004) A survey of iodine content in Laminaria digitata. Bot Mar 47:30

    Google Scholar 

  • Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28(11):1091–1101

    Article  PubMed  CAS  Google Scholar 

  • Glombitza K-W, Gerstberger G (1985) Phlorotannins with dibenzodioxin structural elements from the brown alga Eisenia arborea. Phytochemistry 24(3):543–551

    Article  CAS  Google Scholar 

  • Glombitza K-W, Schmidt A (1999) Nonhalogenated and halogenated phlorotannins from the brown alga Carpophyllum angustifolium. J Nat Prod 62(9):1238–1240

    Article  PubMed  CAS  Google Scholar 

  • Glombitza K-W, Koch M, Eckhardt G (1977) Chlorierte phlorethole aus Laminaria ochroleuca. Phytochemistry 16(6):796–798

    Article  CAS  Google Scholar 

  • Goldberg ED (1963) The oceans as a chemical system. In: Hill MN (ed) The sea, vol 2. John Wiley & Sons, New York, pp 3–20

  • Green D, Kashman Y, Miroz A (1993) Colpol, a new cytotoxic C6-C4-C6 metabolite from the alga Colpomenia sinuosa. J Nat Prod 56(7):1201–1202

    Article  CAS  Google Scholar 

  • Gschwend PM, Macfarlane JK, Newman KA (1985) Volatile halogenated organic compounds released to seawater from temperate marine macroalgae. Science 227(4690):1033–1035

    Article  PubMed  CAS  Google Scholar 

  • Hara I, Sakurai T (1998) Isolation and characterization of vanadium bromoperoxidase from a marine macroalga, Ecklonia stolonifera. J Inorg Biochem 72(1):23–28

    Article  PubMed  CAS  Google Scholar 

  • Hartung J, Brucher O, Hach D, Schulz H, Vilter H, Ruick G (2008) Bromoperoxidase activity and vanadium level of the brown alga Ascophyllum nodosum. Phytochemistry 69(16):2826–2830

    Article  PubMed  CAS  Google Scholar 

  • Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22(15):3803–3815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heyland A, Moroz LL (2005) Cross-kingdom hormonal signaling: an insight from thyroid hormone functions in marine larvae. J Exp Biol 208(23):4355–4361

    Article  PubMed  CAS  Google Scholar 

  • Isupov MN, Dalby AR, Brindley AA, Izumi Y, Tanabe T, Murshudov GN, Littlechild JA (2000) Crystal structure of dodecameric vanadium-dependent bromoperoxidase from the red algae Corallina officinalis. J Mol Biol 299(4):1035–1049

    Article  PubMed  CAS  Google Scholar 

  • Itoh I (1988) Substrate specificity, regiospecificity and stereospecificity of halogenation reactions catalyzed by non-heme-type bromoperoxidase of Corallina piltllifera. Eur J Biochem 172:484

    Article  Google Scholar 

  • Jannun R, Coe EL (1987) Bromoperoxidase from the marine snail, Murex trunculus. Comp Biochem Physiol B 88(3):917–922

    Article  Google Scholar 

  • Jordan P, Kloareg B, Vilter H (1991) Detection of vanadate-dependent bromoperoxidases in protoplasts from the brown algae Laminaria digitata and L. saccharina. J Plant Physiol 137(5):520–524

    Article  CAS  Google Scholar 

  • Kladi M, Vagias C, Roussis V (2004) Volatile halogenated metabolites from marine red algae. Phytochem Rev 3(3):337–366

    Article  CAS  Google Scholar 

  • Koch M, Gregson RP (1984) Brominated phlorethols and nonhalogenated phlorotannins from the brown alga Cystophora congesta. Phytochemistry 23(11):2633–2637

    Article  CAS  Google Scholar 

  • Kongkiattikajorn J, Pongdam S (2006) Vanadium haloperoxidase from the red alga Gracilaria fisheri. Sci Asia 32:25–30

    Article  Google Scholar 

  • Kongkiattikajorna J, Ruenwongsab P, Panijpanb B (2006) Chemical modification of lysine and histidine residues in Gracilaria tenuistipitata bromoperoxidase: effect on stability and activity. ScienceAsia 32(Suppl 1):37–42

  • Kousaka K, Ogi N, Akazawa Y, Fujieda M, Yamamoto Y, Takada Y, Kimura J (2003) Novel oxylipin metabolites from the brown alga Eisenia bicyclis. J Nat Prod 66(10):1318–1323

    Article  PubMed  CAS  Google Scholar 

  • Krenn BE, Plat H, Wever R (1987) The bromoperoxidase from the red alga Ceramium rubrum also contains vanadium as a prosthetic group. Biochim Biophys Acta Protein Struct Mol Enzymol 912(2):287–291

    Article  CAS  Google Scholar 

  • Krenn BE, Plat H, Wever R (1988) Purification and some characteristics of a non-haem bromoperoxidase from Streptomyces aureofaciens. Biochim Biophys Acta Protein Struct Mol Enzymol 952:255–260

    Article  CAS  Google Scholar 

  • Krenn BE, Tromp MG, Wever R (1989) The brown alga Ascophyllum nodosum contains two different vanadium bromoperoxidases. J Biol Chem 264(32):19287–19292

    PubMed  CAS  Google Scholar 

  • Küpper FC, Kroneck PM (2014) Iodine bioinorganic chemistry. Iodine Chemistry and Applications:555–589

  • Küpper F, Schweigert N, Ar Gall E, Legendre J-M, Vilter H, Kloareg B (1998) Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta 207:163–171

    Article  Google Scholar 

  • Küpper FC, Kloareg B, Guern J, Potin P (2001) Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol 125(1):278–291

    Article  PubMed  PubMed Central  Google Scholar 

  • Küpper FC, Müller DG, Peters AF, Kloareg B, Potin P (2002) Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of Laminariales. J Chem Ecol 28(10):2057–2081

    Article  PubMed  Google Scholar 

  • Küpper FC, Gaquerel E, Boneberg E-M, Morath S, Salaün J-P, Potin P (2006) Early events in the perception of lipopolysaccharides in the brown alga Laminaria digitata include an oxidative burst and activation of fatty acid oxidation cascades. J Exp Bot 57(9):1991–1999

    Article  PubMed  CAS  Google Scholar 

  • Küpper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Waite TJ, Boneberg E-M et al (2008) Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proc Natl Acad Sci U S A 105(19):6954–6958

    Article  PubMed  PubMed Central  Google Scholar 

  • Küpper FC, Carpenter LJ, Leblanc C, Toyama C, Uchida Y, Maskrey BH et al (2013) In vivo speciation studies and antioxidant properties of bromine in Laminaria digitata reinforce the significance of iodine accumulation for kelps. J Exp Bot 64(10):2653–2664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lazrus AL, Gandrud BW, Woodard RN, Sedlacek WA (1975) Stratospheric halogen measurements. Geophys Res Lett 2(10):439–441

    Article  CAS  Google Scholar 

  • La Barre S, Potin P, Leblanc C, Delage L (2010) The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Mar Drugs 8(4):988–1010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Laturnus F (2001) Marine macroalgae in polar regions as natural sources for volatile organohalogens. Environ Sci Pollut Res 8(2):103–108

    Article  CAS  Google Scholar 

  • Laturnus F, Giese B, Wiencke C, Adams FC (2000) Low-molecular-weight organoiodine and organobromine compounds released by polar macroalgae—the influence of abiotic factors. Fresenius J Anal Chem 368(2–3):297–302

    Article  PubMed  CAS  Google Scholar 

  • Leblanc C, Colin C, Cosse A, Delage L, La Barre S, Morin P et al (2006) Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie 88(11):1773–1785

    Article  PubMed  CAS  Google Scholar 

  • Leblanc C, Vilter H, Fournier JB, Delage L, Potin P, Rebuffet E et al (2015) Vanadium haloperoxidases: from the discovery 30 years ago to X-ray crystallographic and V K-edge absorption spectroscopic studies. Coord Chem Rev 301–302:134–146

    Article  CAS  Google Scholar 

  • Lee JD, McFiggans G, Allan JD, Baker AR, Ball SM, Benton AK, Carpenter LJ, Commane R, Finley BD, Evans M et al (2009) Iodine-mediated coastal particle formation: an overview of the reactive halogens in the marine boundary layer (RHaMBLe) Roscoff coastal study. Atmos Chem Phys Discuss 9:26421–26489

    Article  Google Scholar 

  • Leedham EC, Hughes C, Keng FSL, Phang SM, Malin G, Sturges WT (2013) Emission of atmospherically significant halocarbons by naturally occurring and farmed tropical macroalgae. Biogeosciences 10(6):3615–3633

    Article  CAS  Google Scholar 

  • Lesser MP (2012) Oxidative stress in tropical marine ecosystems. In: Abele D, Vazquez-Medina JP, Zenteno-Savin T (eds) Oxidative stress in aquatic ecosystems, vol 1. Wiley-Blackwell, Oxford, pp 9–19

  • Littlechild J (1999) Haloperoxidases and their role in biotransformation reactions. Curr Opin Chem Biol 3(1):28–34

    Article  PubMed  CAS  Google Scholar 

  • Littlechild J, Garcia-Rodriguez E (2003) Structural studies on the dodecameric vanadium bromoperoxidase from Corallina species. Coord Chem Rev 237(1):65–76

    Article  CAS  Google Scholar 

  • Littlechild J, Rodriguez EG, Isupov M (2009) Vanadium containing bromoperoxidase—insights into the enzymatic mechanism using X-ray crystallography. J Inorg Biochem 103(4):617–621

    Article  PubMed  CAS  Google Scholar 

  • Lohrmann NL, Logan BA, Johnson AS (2004) Seasonal acclimatization of antioxidants and photosynthesis in Chondrus crispus and Mastocarpus stellatus, two co-occurring red algae with differing stress tolerances. Biol Bull 207(3):225–232

    Article  PubMed  CAS  Google Scholar 

  • Mackey D, McFall AJ (2006) MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol Microbiol 61(6):1365–1371

    Article  PubMed  CAS  Google Scholar 

  • Maharana D, Das PB, Verlecar XN, Pise NM, Gauns M (2015) Oxidative stress tolerance in intertidal red seaweed Hypnea musciformis (Wulfen) in relation to environmental components. Environ Sci Pollut Res Int

  • Malmvärn A, Marsh G, Kautsky L, Athanasiadou M, Bergman Å, Asplund L (2005) Hydroxylated and methoxylated brominated diphenyl ethers in the red algae Ceramium tenuicorne and blue mussels from the Baltic Sea. Environ Sci Technol 39(9):2990–2997

    Article  PubMed  CAS  Google Scholar 

  • Manthey J, Hager L (1981) Purification and properties of bromoperoxidase from Penicillus capitatus. J Biol Chem 256(21):11232–11238

    PubMed  CAS  Google Scholar 

  • Mata L, Gaspar H, Santos R (2012) Carbon/nutrient balance in relation to biomass production and halogenated compound content in the red alga Asparagopsis taxiformis (Bonnemaisoniaceae) 1. J Phycol 48(1):248–253

    Article  PubMed  CAS  Google Scholar 

  • Maurya M (2006) Structural models of vanadate-dependent haloperoxidases and their reactivity. J Chem Sci 118(6):503–511

    Article  CAS  Google Scholar 

  • Maximilien R, de Nys R, Holmström C, Gram L, Givskov M, Crass K et al (1998) Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Ecol 15(3):233–246

    Article  Google Scholar 

  • McFiggans G, Coe H, Burgess R, Allan J, Cubison M, Alfarra MR et al (2004) Direct evidence for coastal iodine particles from Laminaria macroalgae—linkage to emissions of molecular iodine. Atmos Chem Phys 4(3):701–713

    Article  CAS  Google Scholar 

  • Mehrtens G, Laturnus F (1998) Halogenating activity in an arctic population of brown macroalga Laminaria saccharina (L.) Lamour. Oceanogr Lit Rev 2(45):351

    Google Scholar 

  • Meister GE, Butler A (1994) Molybdenum(VI)- and tungsten(VI)-mediated biomimetic chemistry of vanadium bromoperoxidase. Inorg Chem 33(15):3269–3275

    Article  CAS  Google Scholar 

  • Messerschmidt A, Wever R (1996) X-ray structure of a vanadium-containing enzyme: chloroperoxidase from the fungus Curvularia inaequalis. Proc Natl Acad Sci 93(1):392–396

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milkova T, Talev G, Christov R, Dimitrova-Konaklieva S, Popov S (1997) Sterols and volatiles in Cystoseira barbata and Cystoseira crinita from the Black Sea. Phytochemistry 45(1):93–95

    Article  CAS  Google Scholar 

  • Mithöfer A, Schulze B, Boland W (2004) Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 566(1–3):1–5

    Article  PubMed  CAS  Google Scholar 

  • Neidleman SL (1975) Microbial halogenation. CRC Crit Rev Microbiol 3(4):333–358

    Article  PubMed  CAS  Google Scholar 

  • Neidleman SL, Geigert J (1986) Biohalogenation: principles, basic roles, and applications. Ellis Horwood Ltd., Chichester

  • Neilson AH (2003) Biological effects and biosynthesis of brominated metabolites. In: Neilson AH (ed) The handbook of environmental chemistry, vol 3. Springer, Berlin, pp 75–204

  • Nightingale PD, Malin G, Liss P (1995) Production of chloroform and other low molecular-weight halocarbons by some species of macroalgae. Limnol Oceanogr 40(4):680–689

    Article  CAS  Google Scholar 

  • O’Dowd CD, Hoffmann T (2006) Coastal new particle formation: a review of the current state-of-the-art. Environ Chem 2(4):245–255

    Article  CAS  Google Scholar 

  • O’Dowd C, McFiggans G, Creasey DJ, Pirjola L, Hoell C, Smith MH et al (1999) On the photochemical production of new particles in the coastal boundary layer. Geophys Res Lett 26(12):1707–1710

    Article  Google Scholar 

  • O’Dowd CD, Jimenez JL, Bahreini R, Flagan RC, Seinfeld JH, Hämeri K et al (2002) Marine aerosol formation from biogenic iodine emissions. Nature 417(6889):632–636

    Article  PubMed  CAS  Google Scholar 

  • Ohshiro T, Nakano S, Takahashi Y, Suzuki M, Izumi Y (1999) Occurrence of bromoperoxidase in the marine green macro-alga, Ulvella lens, and emission of volatile brominated methane by the enzyme. Phytochemistry 52(7):1211–1215

    Article  CAS  Google Scholar 

  • Orfanidis S (1992) Light requirements for growth of six shade-acclimated Mediterranean macroalgae. Mar Biol 112(3):511–515

    Article  Google Scholar 

  • Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13(1):179–191

    Article  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Bermúdez P, Srebotnik E, Hammel KE (2003) Chlorination and cleavage of lignin structures by fungal chloroperoxidases. Appl Environ Microbiol 69(8):5015–5018

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palmer CJ, Anders TL, Carpenter LJ, Küpper FC, McFiggans GB (2005) Iodine and halocarbon response of to oxidative stress and links to atmospheric new particle production. Environ Chem 2(4):282

  • Pang AH, Garneau-Tsodikova S, Tsodikov OV (2015) Crystal structure of halogenase PltA from the pyoluteorin biosynthetic pathway. J Struct Biol 192(3):349–357

    Article  PubMed  CAS  Google Scholar 

  • Parameswaran P, Bhat K, Das B, Kamat S, Harnos S (1994) Halogenated terpenoids from the brown alga Padina tetrastromatica (Hauck), vol 33. Council Scientific Industrial Research Publ & Info Directorate, New Delhi, pp 1006–1008

  • Pedersén M (1976) A brominating and hydroxylating peroxidase from the red alga Cystoclonium purpureum. Physiol Plant 37(1):6–11

    Article  Google Scholar 

  • Phang S-M, Keng FS-L, Paramjeet-Kaur MS, Lim Y-K-A, Rahman NA, Leedham EC et al (2016) Can seaweed farming in the tropics contribute to climate change through emission of short-lived halocarbons? MJS 34(1):8–19

  • Plass W (2009) Vanadium haloperoxidases as supramolecular hosts: synthetic and computational models. Pure Appl Chem 81(7):1229–1239

    Article  CAS  Google Scholar 

  • Plat H, Krenn BE, Wever R (1987) The bromoperoxidase from the lichen Xanthoria parietina is a novel vanadium enzyme. Biochem J 248(1):277–279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Potin P, Leblanc C (2006) Phenolic-based adhesives of marine brown algae. In: Smith A, Callow J (eds) Biological adhesives. Springer, Berlin, pp 105–124

    Chapter  Google Scholar 

  • Quack B, Atlas E, Petrick G, Stroud V, Schauffler S, Wallace DW (2004) Oceanic bromoform sources for the tropical atmosphere. Geophys Res Lett 31(23)

  • Raugei S, Carloni P (2006) Structure and function of vanadium haloperoxidases. J Phys Chem B 110(8):3747–3758

    Article  PubMed  CAS  Google Scholar 

  • Rehder D (1999) The coordination chemistry of vanadium as related to its biological functions. Coord Chem Rev 182(1):297–322

    Article  Google Scholar 

  • Rehder D, Hoist H, Priebsch W, Vuter H (1991) Vanadate-dependent bromo/iodoperoxidase from ascophyllum nodosum also contains unspecific low-affinity binding sites for vanadate (V): a 51V NMR investigation, including the model peptides Phe-Glu and Gly-Tyr. J Inorg Biochem 41(3):171–185

    Article  CAS  Google Scholar 

  • Renirie R, Hemrika W, Wever R (2000) Peroxidase and phosphatase activity of active-site mutants of vanadium chloroperoxidase from the fungus Curvularia inaequalis. Implications for the catalytic mechanisms. J Biol Chem 275(16):11650–11657

    Article  PubMed  CAS  Google Scholar 

  • Ritter A, Ubertini M, Romac S, Gaillard F, Delage L, Mann A et al (2010) Copper stress proteomics highlights local adaptation of two strains of the model brown alga Ectocarpus siliculosus. Proteomics 10(11):2074–2088

    Article  PubMed  CAS  Google Scholar 

  • Roeder V, Collén J, Rousvoal S, Corre E, Leblanc C, Boyen C (2005) Identification of stress gene transcripts in Laminaria digitata (Phaeophyceae) protoplast cultures by expressed sequence tag analysis. J Phycol 41(6):1227–1235

    Article  CAS  Google Scholar 

  • Rorrer GL, Tucker MP, Cheney DP, Maliakal S (2001) Bromoperoxidase activity in microplantlet suspension cultures of the macrophytic red alga Ochtodes secundiramea. Biotechnol Bioeng 74(5):389–395

    Article  PubMed  CAS  Google Scholar 

  • Ross C, Alstyne KLV (2007) Intraspecific variation in stress-induced hydrogen peroxide scavenging by the ulvoid macroalga Ulva lactuca. J Phycol 43(3):466–474

    Article  Google Scholar 

  • Rush C, Willetts A, Davies G, Dauter Z, Watson H, Littlechild J (1995) Purification, crystallisation and preliminary X-ray analysis of the vanadium-dependent haloperoxidase from Corallina officinalis. FEBS Lett 359(2–3):244–246

    Article  PubMed  CAS  Google Scholar 

  • Saenko G, Kravtsova Y, Ivanenko V, Sheludko S (1978) Concentration of iodine and bromine by plants in the seas of Japan and Okhotsk. Mar Biol 47(3):243–250

    Article  Google Scholar 

  • Saiz-Lopez A, Lamarque J-F, Kinnison D, Tilmes S, Ordóñez C, Orlando J et al (2012) Estimating the climate significance of halogen-driven ozone loss in the tropical marine troposphere. Atmos Chem Phys 12(9):3939–3949

    Article  CAS  Google Scholar 

  • Saiz-Lopez A, Shillito JA, Coe H, Plane JMC (2006) Measurements and modelling of I2 IO, OIO, BrO and NO3 in the mid-latitude marine boundary layer. Atmos Chem Phys 6(6):1513–1528

    Article  CAS  Google Scholar 

  • Salaün S, La Barre S, Dos Santos-Goncalvez M, Potin P, Haras D, Bazire A (2012) Influence of exudates of the kelp Laminaria digitata on biofilm formation of associated and exogenous bacterial epiphytes. Microb Ecol 64(2):359–369

    Article  PubMed  Google Scholar 

  • Salawitch RJ (2006) Atmospheric chemistry: biogenic bromine. Nature 439(7074):275–277

    Article  PubMed  CAS  Google Scholar 

  • Sandy M, Carter-Franklin JN, Martin JD, Butler A (2011) Vanadium bromoperoxidase from Delisea pulchra: enzyme-catalyzed formation of bromofuranone and attendant disruption of quorum sensing. Chem Commun 47(44):12086–12088

    Article  CAS  Google Scholar 

  • Shibata T, Hama Y, Miyasaki T, Ito M, Nakamura T (2006) Extracellular secretion of phenolic substances from living brown algae. J Appl Phycol 18(6):787–794

    Article  CAS  Google Scholar 

  • Shimonishi M, Kuwamoto S, Inoue H, Wever R, Ohshiro T, Izumi Y, Tanabe T (1998) Cloning and expression of the gene for a vanadium-dependent bromoperoxidase from a marine macro-alga, Corallina pilulifera. FEBS Lett 428(1):105–110

    Article  PubMed  CAS  Google Scholar 

  • Sigel A, Sigel H (1995) Metal ions in biological systems: volume 31: vanadium and its role for life. CRC, Boca Raton

    Google Scholar 

  • Slebodnick C, Hamstra BJ, Pecoraro VL (1997) Modeling the biological chemistry of vanadium: structural and reactivity studies elucidating biological function. In: Sadler PJ (ed) Metal sites in proteins and models, vol 89. Springer, Berlin, pp 51–108

  • Soedjak HS, Butler A (1990) Characterization of vanadium bromoperoxidase from Macrocystis and Fucus: reactivity of vanadium bromoperoxidase toward acyl and alkyl peroxides and bromination of amines. Biochemistry 29(34):7974–7981

    Article  PubMed  CAS  Google Scholar 

  • Soedjak HS, Butler A (1991) Mechanism of dioxygen formation catalyzed by vanadium bromoperoxidase from Macrocystis pyrifera and Fucus distichus: steady state kinetic analysis and comparison to the mechanism of V-BrPO from Ascophyllum nodosum. Biochim Biophys Acta 1079(1):1–7

    Article  PubMed  CAS  Google Scholar 

  • Strittmatter M, Grenville-Briggs LJ, Breithut L, Van West P, Gachon CM, Küpper FC (2016) Infection of the brown alga Ectocarpus siliculosus by the oomycete Eurychasma dicksonii induces oxidative stress and halogen metabolism. Plant Cell Environ 39(2):259–271

    Article  PubMed  CAS  Google Scholar 

  • Suthiphongchai T, Boonsiri P, Panijpan B (2008) Vanadium-dependent bromoperoxidases from Gracilaria algae. J Appl Phycol 20(3):271–278

    Article  CAS  Google Scholar 

  • Tanaka N, Hasan Z, Wever R (2003) Kinetic characterization of active site mutants Ser402Ala and Phe397His of vanadium chloroperoxidase from the fungus Curvularia inaequalis. Inorg Chim Acta 356:288–296

    Article  CAS  Google Scholar 

  • Tarakhovskaya E (2014) Mechanisms of bioadhesion of macrophytic algae. Russ J Plant Physiol 61(1):19–25

    Article  CAS  Google Scholar 

  • Tarakhovskaya ER, Bilova TE, Maslov YI (2015) Hydrogen peroxide content and vanadium-dependent haloperoxidase activity in thalli of six species of Fucales (Phaeophyceae). Phycologia 54(4):417–424

    Article  CAS  Google Scholar 

  • ten Brink HB, Tuynman A, Dekker HL, Hemrika W, Izumi Y, Oshiro T, Wever R (1998) Enantio selective sulfoxidation catalyzed by vanadium haloperoxidases. Inorg Chem 37(26):6780–6784

    Article  PubMed  Google Scholar 

  • Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279(6):L1005–L1028

    Article  PubMed  CAS  Google Scholar 

  • Todd JS, Proteau PJ, Gerwick WH (1993) Egregiachlorides AC: new chlorinated oxylipins from the marine brown alga Egregia menziesii. Tetrahedron Lett 34(48):7689–7692

    Article  CAS  Google Scholar 

  • Tromp MG, Krenn BE, Wever R (1990) Some structural aspects of vanadium bromoperoxidase from Ascophyllum nodosum. Biochim Biophys Acta Protein Struct Mol Enzymol 1040(2):192–198

    Article  CAS  Google Scholar 

  • Van Pee K-H, Lingens F (1985) Purification of bromoperoxidase from Pseudomonas aureofaciens. J Bacteriol 161(3):1171–1175

    PubMed  PubMed Central  Google Scholar 

  • Verhaeghe E, Fraysse A, Guerquin-Kern J-L, Wu T-D, Devès G, Mioskowski C, Potin P (2008a) Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. JBIC J Biol Inorg Chem 13(2):257–269

    Article  PubMed  CAS  Google Scholar 

  • Verhaeghe E, Buisson D, Zekri E, Leblanc C, Potin P, Ambroise Y (2008b) A colorimetric assay for steady-state analyses of iodo-and bromoperoxidase activities. Anal Biochem 379(1):60–65

    Article  PubMed  CAS  Google Scholar 

  • Vilter H (1984) Peroxidases from Phaeophyceae: a vanadium (V)-dependent peroxidase from Ascophyllum nodosum. Phytochemistry 23(7):1387–1390

    Article  CAS  Google Scholar 

  • Vilter H (1995) Vanadium and its role in life. Met Ions Biol Syst 31:325–362

    PubMed  CAS  Google Scholar 

  • Vreeland V, Waite JH, Epstein L (1998) Minireview—Polyphenols and oxidases in substratum adhesion by marine algae and mussels. J Phycol 34(1):1–8

    Article  CAS  Google Scholar 

  • Walker JV, Butler A (1996) Vanadium bromoperoxidase-catalyzed oxidation of thiocyanate by hydrogen peroxide. Inorg Chim Acta 243(1):201–206

    Article  CAS  Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    Article  PubMed  CAS  Google Scholar 

  • Weinberger F, Friedlander M (2000) Endogenous and exogenous elicitors of a hypersensitive response in Gracilaria conferta (Rhodophyta). J Appl Phycol 12(2):139–145

    Article  CAS  Google Scholar 

  • Weinberger F, Richard C, Kloareg B, Kashman Y, Hoppe HG, Friedlander M (2001) Structure-activity relationships of oligoagar elicitors toward Gracilaria conferta (Rhodophyta). J Phycol 37(3):418–426

    Article  CAS  Google Scholar 

  • Weinberger F, Leonardi P, Miravalles A, Correa JA, Lion U, Kloareg B, Potin P (2005a) Dissection of two distinct defense-related responses to agar oligosaccharides in Gracilaria chilensis (Rhodophyta) and Gracilaria conferta (Rhodophyta) 1. J Phycol 41(4):863–873

    Article  CAS  Google Scholar 

  • Weinberger F, Pohnert G, Berndt M-L, Bouarab K, Kloareg B, Potin P (2005b) Apoplastic oxidation of L-asparagine is involved in the control of the green algal endophyte Acrochaete operculata Correa & Nielsen by the red seaweed Chondrus crispus Stackhouse. J Exp Bot 56(415):1317–1326

    Article  PubMed  CAS  Google Scholar 

  • Weinberger F, Coquempot B, Forner S, Morin P, Kloareg B, Potin P (2007) Different regulation of haloperoxidation during agar oligosaccharide-activated defence mechanisms in two related red algae, Gracilaria sp and Gracilaria chilensis. J Exp Bot 58(15–16):4365–4372

    Article  PubMed  CAS  Google Scholar 

  • Wever R (2012) Structure and function of vanadium haloperoxidases. In: Michibata H (ed) Vanadium. Springer, Dordrecht, pp 95–125

    Chapter  Google Scholar 

  • Wever R, Hemrika W (2001) Vanadium haloperoxidases. Handbook of metalloproteins, pp 1417–1428

  • Wever R, van der Horst MA (2013) The role of vanadium haloperoxidases in the formation of volatile brominated compounds and their impact on the environment. Dalton Trans 42(33):11778–11786

    Article  PubMed  CAS  Google Scholar 

  • Wever R, Plat H, de Boer E (1985) Isolation procedure and some properties of the bromoperoxidase from the seaweed Ascophyllum nodosum. Biochim Biophys Acta Protein Struct Mol Enzymol 830(2):181–186

    Article  CAS  Google Scholar 

  • Weyand M, Hecht H, Kiess M, Liaud M, Vilter H, Schomburg D (1999) X-ray structure determination of a vanadium-dependent haloperoxidase from Ascophyllum nodosum at 2.0 A resolution. J Mol Biol 293(3):595–611

    Article  PubMed  CAS  Google Scholar 

  • Winter JM, Moore BS (2009) Exploring the chemistry and biology of vanadium-dependent haloperoxidases. J Biol Chem 284(28):18577–18581

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wischang D, Hartung J (2012) Bromination of phenols in bromoperoxidase-catalyzed oxidations. Tetrahedron 68(46):9456–9463

    Article  CAS  Google Scholar 

  • Wischang D, Brücher O, Hartung J (2011) Bromoperoxidases and functional enzyme mimics as catalysts for oxidative bromination—a sustainable synthetic approach. Coord Chem Rev 255(19):2204–2217

    Article  CAS  Google Scholar 

  • Wischang D, Radlow M, Schulz H, Vilter H, Viehweger L, Altmeyer MO, Gaillard F (2012) Molecular cloning, structure, and reactivity of the second bromoperoxidase from Ascophyllum nodosum. Bioorg Chem 44:25–34

    Article  PubMed  CAS  Google Scholar 

  • Wofsy SC, McElroy MB, Yung YL (1975) The chemistry of atmospheric bromine. Geophys Res Lett 2(6):215–218

    Article  CAS  Google Scholar 

  • Wu H, Song Z, Hentzer M, Andersen JB, Molin S, Givskov M, Høiby N (2004) Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53(6):1054–1061

    Article  PubMed  CAS  Google Scholar 

  • Xu G, Wang B-G (2016) Independent evolution of six families of halogenating enzymes. PLoS One 11(5):e0154619

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yende SR, Harle UN, Chaugule BB (2014) Therapeutic potential and health benefits of Sargassum species. Pharmacogn Rev 8(15):1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yokouchi Y, Hasebe F, Fujiwara M, Takashima H, Shiotani M, Nishi N et al (2005) Correlations and emission ratios among bromoform, dibromochloromethane, and dibromomethane in the atmosphere. J Geophys Res Atmos (1984–2012) 110(D23)

  • Yu H, Whittaker JW (1989) Vanadate activation of bromoperoxidase from Corallina officinalis. Biochem Biophys Res Commun 160(1):87–92

    Article  PubMed  CAS  Google Scholar 

  • Zambounis A, Strittmatter M, Gachon CM (2013) Chronic stress and disease resistance in the genome model marine seaweed Ectocarpus siliculosus. Aquat Bot 104:147–152

    Article  CAS  Google Scholar 

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Funding

This research is supported by the HICoE MOHE: IOES-2014F Grant; HICoE MOHE: IOES-2014 (Air-ocean-land Interaction); UMCoE RU Grant: RU009-2015 (Air-ocean-land Interaction) and RU009K-2015 (Knowledge Management); UMCoE RU Grant: RU012-2016 (IOES) and GC Grant (GC002A/B/-15SBS).

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Authors and Affiliations

  1. Institute of Ocean and Earth Sciences, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Thillai Punitha & Siew-Moi Phang

  2. Institute of Graduate Studies, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Thillai Punitha

  3. Institute of Biological Sciences, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Siew-Moi Phang

  4. Nanotechnology and Catalysis Research Centre (NANOCAT), University of Malaya, Level 3, IPS Building, Kuala Lumpur, Malaysia

    Joon Ching Juan

  5. School of Science, Monash University Malaysia Campus, Bandar Sunway, 46150, Subang Jaya, Malaysia

    Joon Ching Juan

  6. School of Biological Sciences, Monash University, Clayton, VIC, 3800, Australia

    John Beardall

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Punitha, T., Phang, SM., Juan, J.C. et al. Environmental Control of Vanadium Haloperoxidases and Halocarbon Emissions in Macroalgae. Mar Biotechnol 20, 282–303 (2018). https://doi.org/10.1007/s10126-018-9820-x

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