In vivo speciation studies and antioxidant properties of bromine in Laminaria digitata reinforce the significance of iodine accumulation for kelps

Journal of Experimental Botany

Volumn 64, Issue 10, 2013, Pages 2653-2664

  Küpper, Frithjof C ^a,b   Carpenter, Lucy J ^c   Leblanc, Catherine ^d,e   Toyama, Chiaki ^f   Uchida, Yuka ^f   Maskrey, Benjamin H ^g   Robinson, Joanne ^b   Verhaeghe, Elodie F ^d,e,h   Malin, Gill ⁱ   Luther, George W ^j   Kroneck, Peter M H ^k   Kloareg, Bernard ^d,e   Meyer Klaucke, Wolfram ^l   Muramatsu, Yasuyuki ^f   Megson, Ian L ^g   Potin, Philippe ^d,e   Feiters, Martin C ^m  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b SCOTTISH MARINE INSTITUTE   (United Kingdom)

^c UNIVERSITY OF YORK   (United Kingdom)

^d CNRS   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f GAKUSHUIN UNIVERSITY   (Japan)

^g UNIVERSITY OF THE HIGHLANDS AND ISLANDS   (United Kingdom)

^h SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

ⁱ UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^j UNIVERSITY OF DELAWARE   (United States)

^k UNIVERSITY OF KONSTANZ   (Germany)

^l EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^m RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

more..

Author keywords

Antioxidant; brown algae; electron paramagnetic resonance; halocarbons; reactive oxygen species; X ray absorption spectroscopy.

Indexed keywords

ANTIOXIDANT; BROMINE; IODIDE PEROXIDASE; IODINE; REACTIVE OXYGEN METABOLITE; VANADIUM IODOPEROXIDASE;

ARTICLE; BROWN ALGA; CHEMISTRY; ELECTRON SPIN RESONANCE; GENETICS; HALOCARBONS; KELP; LAMINARIA; METABOLISM; X-RAY ABSORPTION SPECTROSCOPY.;

ANTIOXIDANT; BROWN ALGAE; ELECTRON PARAMAGNETIC RESONANCE; HALOCARBONS; REACTIVE OXYGEN SPECIES; X-RAY ABSORPTION SPECTROSCOPY.;

ANTIOXIDANTS; BROMINE; IODIDE PEROXIDASE; IODINE; KELP; LAMINARIA;

ALGAE; LAMINARIA; LAMINARIA DIGITATA; LAMINARIALES; PHAEOPHYCEAE;

EID: 84879927379     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert110     Document Type: Article

References (64)

1. Ar Gall E, Küpper FC, Kloareg B. 2004. A survey of iodine contents in Laminaria digitata. Botanica Marina 47, 30-37
2. Balard AJ. 1826. Sur une substance particulière contenue dans l'eau de la mer. Annales de Chimie et de Physique (Paris) 32, 337-384
3. Baldauf SL. 2003. The deep roots of eukaryotes. Science 300, 1703-1706
4. Bhattacharya D, Stickel SK, Sogin ML. 1991. Molecular phylogenetic analysis of actin genic regions from Achlya bisexualis (Oomycota) and Costaria costata (Chromophyta). Journal of Molecular Evolution 33, 525-536
5. Bichsel Y, von Gunten U. 1999. Oxidation of iodide and hypoiodous acid in the disinfection of natural waters. Environmental Science and Technology 33, 4040-4045
6. Bielski BHJ, Cabelli DE, Arudi RL, Ross AB. 1985. Reactivity of HO2/O2-radicals in aqueous solution. Journal of Physical and Chemical Reference Data 14, 1041-1100
7. Butler A, Carter-Franklin JN. 2004. The role of vanadium bromoperoxidase in the biosynthesis of halogenated marine natural products. Natural Product Reports 21, 180-188
8. Buxton GV, Greenstock CL, Helman WP, Ross AB. 1988. Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals in aqueous solution. Journal of Physical and Chemical Reference Data 17, 513-886
9. Carpenter LJ, Hopkins JR, Jones CE, Lewis AC, Parthipan R, Wevill DJ, Poissant L, Pilote M, Constant P. 2005. Abiotic source of CH2I2 and other reactive organic halogens in the sub-Arctic atmosphere? Environmental Science and Technology 39, 8812-8816
10. Carpenter LJ, Jones CE, Dunk RM, Hornsby KE, Woeltjen J. 2009. Air-sea fluxes of biogenic bromine from the tropical and North Atlantic Ocean. Atmospheric Chemistry and Physics 9, 1805-1816
11. Carpenter LJ, Liss PS. 2000. On temperate sources of bromoform and other reactive organic bromine gases. Journal of Geophysical Research-Atmospheres 105, 20539-20547
12. Carpenter LJ, Malin G, Küpper FC, Liss PS. 2000. Novel biogenic iodine-containing trihalomethanes and other short-lived halocarbons in the coastal East Atlantic. Global Biogeochemical Cycles 14, 1191-1204
13. Chai JY, Muramatsu Y. 2007. Determination of bromine and iodine in twenty-three geochemical reference materials by ICP-MS. Geostandards and Geoanalytical Research 31, 143-150
14. Chance R, Baker AR, Küpper FC, Hughes C, Kloareg B, Malin G. 2009. Release and transformations of inorganic iodine by marine macroalgae. Estuarine Coastal and Shelf Science 82, 406-414
15. Cock JM, Sterck L, Rouzé P, et al. 2010. The Ectocarpus genome and the independent evolution of multicellularity in the brown algae. Nature 465, 617-621
16. 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. Journal of Biological Inorganic Chemistry 10, 156-166
17. Colin C, Leblanc C, Wagner E, Delage L, Leize-Wagner E, Van Dorsselaer A, Kloareg B, Potin P. 2003. The brown algal kelp Laminaria digitata features distinct bromoperoxidase and iodoperoxidase activities. Journal of Biological Chemistry 278, 23545-23552
18. Collén J, Del Rio MJ, Garcia-Reina G, Pedersén M. 1996. Photosynthetic H2O2 production by Ulva rigida. Planta 196, 225-239
19. Connan S, Delisle F, Deslandes E, Gall EA. 2006. Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Botanica Marina 49, 39-46
20. Cosse A, Potin P, Leblanc C. 2009. Patterns of gene expression induced by oligoguluronates reveal conserved and environmentspecific molecular defense responses in the brown alga Laminaria digitata. New Phytologist 182, 239-250
21. D'Autréaux B, Toledano MB. 2007. ROS as signalling molecules: Mechanisms that generate specificity in ROS homeostasis. Nature Reviews Molecular Cell Biology 8, 813-824
22. Feiters MC, Küpper FC, Meyer-Klaucke W. 2005a. X-ray absorption spectroscopic studies on model compounds for biological iodine and bromine. Journal of Synchrotron Radiation 12, 85-93
23. Feiters MC, Leblanc C, Küpper FC, Meyer-Klaucke W, Michel G, Potin P. 2005b. Bromine is an endogenous component of a vanadium bromoperoxidase. Journal of the American Chemical Society 127, 15340-15341
24. Flohe L, Loschen G, Günzler WA, Eichele E. 1972. Glutathione peroxidase, V. The kinetic mechanism. Hoppe-Seyler's Zeitschrift für Physiologische Chemie 353, 987-999
25. Gay-Lussac L-J. 1813. Sur un nouvel acide formé avec la substance découverte par M. Courtois. Annales de Chimie (Paris) 88, 311-318
26. Hoigné J, Bader H, Haag WR, Staehelin J. 1985. Rate constants of reactions of ozone with organic and inorganic compounds in water-III. Inorganic compounds and radicals. Water Research 19, 993-1004
27. Kanofsky JR, Sima PD. 1995. Reactive absorption of ozone by aqueous biomolecule solutions-implications for the role of sulfhydryl compounds as targets for ozone. Archives of Biochemistry and Biophysics 315, 52-62
28. Küpper FC, Carpenter LJ, McFiggans GB, et al. 2008. Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proceedings of the National Academy of Sciences, USA 105, 6954-6958
29. Küpper FC, Feiters MC, Olofsson B, et al. 2011. Commemorating two centuries of iodine research: An interdisciplinary overview of current research. Angewandte Chemie-International Edition 50, 11598-11620
30. 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. Journal of Experimental Botany 57, 1991-1999
31. Küpper FC, Gaquerel E, Cosse A, Adas F, Peters AF, Müller DG, Kloareg B, Salaün JP, Potin P. 2009. Free fatty acids and methyl jasmonate trigger defense reactions in Laminaria digitata. Plant and Cell Physiology 50, 789-800
32. Küpper FC, Kloareg B, Guern J, Potin P. 2001. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiology 125, 278-291
33. 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 the sporophytes of Laminariales. Journal of Chemical Ecology 28, 2057-2081
34. Küpper FC, Schweigert N, Ar Gall E, Legendre JM, Vilter H, Kloareg B. 1998. Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta 207, 163-171
35. La Barre S, Potin P, Leblanc C, Delage L. 2010. The halogenated metabolism of brown algae (Phaeophyta), its biological importance and its environmental significance. Marine Drugs 8, 988-1010
36. Liu Q, Schurter LM, Muller CE, Aloisio S, Francisco JS, Margerum DW. 2001. Kinetics and mechanisms of aqueous ozone reactions with bromide, sulfite, hydrogen sulfite, iodide, and nitrite ions. Inorganic Chemistry 40, 4436-4442
37. Long LH, Halliwell B. 2001. Antioxidant and prooxidant abilities of foods and beverages. Flavonoids and Other Polyphenols 335, 181-190
38. Luther III GW. 2011. Thermodynamic redox calculations for one and two electron transfer steps: Implications for halide oxidation and halogen environmental cycling. In: P Tratnyek, T Grundl, SB Haderlein, eds, Aquatic redox chemistry, vol. 1071. Washington, DC: American Chemical Society, pp 15-35
39. Mabeau S, Kloareg B. 1987. Isolation and analysis of the cell walls of brown algae: Fucus spiralis, F. ceranoides, F. vesiculosus, F. serratus, Bifurcaria bifurcata and Laminaria digitata. Journal of Experimental Botany 38, 1573-1580
40. McFiggans GB, Coe H, Burgess R, et al. 2004. Direct evidence for coastal iodine particles from Laminaria macroalgae-linkage to emissions of molecular iodine. Atmospheric Chemistry and Physics 4, 701-713
41. McHugh DJ. 1987. Production, properties and uses of alginates. In: DJ McHugh, ed, Production and utilization of products from commercial seaweeds . Rome: FAO, pp 58-115
42. Meja KK, Rajendrasozhan S, Adenuga D, et al. 2008. Curcumin restores corticosteroid function in monocytes exposed to oxidants by maintaining HDAC2. American Journal of Respiratory Cell and Molecular Biology 39, 312-323
43. Mohammed A, Liebhafsky HA. 1934. The kinetics of the reduction of hydrogen peroxide by the halides. Journal of the American Chemical Society 56, 1680-1685
44. Palmer CJ, Anders TL, Carpenter LJ, Küpper FC, McFiggans GB. 2005. Iodine and halocarbon response of Laminaria digitata to oxidative stress and links to atmospheric new particle production. Environmental Chemistry 2, 282-290
45. Polle A, Junkermann W. 1996. Inhibition of apoplastic and symplastic peroxidase activity from Norway spruce by the photooxidant hydroxymethyl hydroperoxide. Plant Physiology 104, 617-623
46. Potin P, Leblanc C. 2006. Phenolic-based adhesives of marine brown algae. In: AM Smith, JA Callow, eds, Biological adhesives. Berlin and Heidelberg: Springer Verlag, pp 105-124
47. Repine JE, White JG, Clawson CC, Holmes BM. 1974. Effects of phorbol myristate acetate on metabolism and ultrastructure of neutrophils in chronic granulomatous disease. Journal of Clinical Investigation 54, 83-90
48. Rosenthal I, Frimer, A. 1976. The quenching effect of iodide ion on singlet oxygen. Photochemistry and Photobiology 23, 209-211
49. Saenko GN, Kravtsova YY, Ivanenko VV, Sheludko SI. 1978. Concentration of iodine and bromine by plants in the seas of Japan and Okhotsk. Marine Biology 47, 243-250
50. Schnetger B, Muramatsu Y. 1996. Determination of halogens, with special reference to, iodine, in geological and biological samples using pyrohydrolysis for preparation and inductively coupled plasma mass spectrometry and ion chromatography for measurement. Analyst 121, 1627-1631
51. Strange RW, Feiters MC. 2008. Biological X-ray absorption spectroscopy (BioXAS): A valuable tool for the study of trace elements in the life sciences. Current Opinion in Structural Biology 18, 1-8
52. Sunda W, Kieber DJ, Kiene RP, Huntsman S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418, 317-320
53. Tanida T, Watanabe I. 2000. Dependence of EXAFS (Extended X-Ray Absorption Fine Structure) parameters of iodide anions in various solvents upon a solvent parameter. Bulletin of the Chemical Society of Japan 73, 2747-2752
54. Theiler R, Cook JC, Hager LP, Studa JF. 1978. Halohydrocarbon synthesis by bromoperoxidase. Science 202, 1094-1096
55. Thomas F, Cosse A, Goulitquer S, Raimund S, Morin P, Valero M, Leblanc C, Potin P. 2011. Waterborne signaling primes the expression of elicitor-induced genes and buffers the oxidative responses in the brown alga Laminaria digitata. PLOS One 6, e21475
56. Truesdale VW, Luther GW, Canosamas C. 1995. Molecular-iodine reduction in seawater-an improved rate-equation considering organic compounds. Marine Chemistry 48, 143-150
57. Venturi S, Venturi M. 1999. Iodide, thyroid and stomach carcinogenesis: Rvolutionary story of a primitive antioxidant? European Journal of Endocrinology 140, 371-372
58. Verhaeghe E, Buisson D, Zekri E, Leblanc C, Potin P, Ambroise Y. 2008a. A colorimetric assay for steady-state analyses of iodo-and bromoperoxidase activities. Analytical Biochemistry 379, 60-65
59. Verhaeghe EF, Fraysse A, Guerquin-Kern J-L, Wu T-D, Devès G, Mioskowski C, Leblanc C, Ortega R, Ambroise Y, Potin P. 2008b. Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. Journal of Biological Inorganic Chemistry 13, 257-269
60. Vilter H. 1995. Vanadium-dependent haloperoxidases In: H Sigel, A Sigel, eds, Vanadium and its role in life, vol. 31. New York: Marcel Dekker, pp 325-362
61. Weiss SJ, Test ST, Eckmann CM, Roos D, Regiani S. 1986. Brominating oxidants generated by human eosinophils. Science 234, 200-203
62. Wilkinson F, Helman WP, Ross AB. 1995. Rate constants for the decay and reactions of the lowest electronically excited singlet state of molecular oxygen in solution. An expanded and revised compilation. Journal of Physical and Chemical Reference Data 24, 663-1023
63. Wojtaszek P. 1997. Oxidative burst: An early plant response to pathogen infection. The Biochemical Journal 322, 681-692
64. Zambounis A, Gaquerel E, Strittmatter M, Potin P, Küpper FC. 2012. Prostaglandin A2 triggers a strong oxidative burst in Laminaria: A novel defense inducer in brown algae? Algae 27, 1-12