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

• Published in: Journal of experimental botany Vol. 64; no. 10; pp. 2653 - 2664
• Main Authors: Küpper, Frithjof C, Carpenter, Lucy J, Leblanc, Catherine, Toyama, Chiaki, Uchida, Yuka, Maskrey, Benjamin H, Robinson, Joanne, Verhaeghe, Elodie F, Malin, Gill, Luther, George W, Kroneck, Peter M. H, Kloareg, Bernard, Meyer-Klaucke, Wolfram, Muramatsu, Yasuyuki, Megson, Ian L, Potin, Philippe, Feiters, Martin C
• Format: Journal Article
• Language: English
• Published: Oxford Oxford University Press [etc.] 01-07-2013; Oxford University Press
• Subjects: absorption; antioxidant activity; antioxidants; Antioxidants - metabolism; Biological and medical sciences; bromine; Bromine - analysis; Bromine - metabolism; chemical speciation; Fundamental and applied biological sciences. Psychology; Iodide Peroxidase - genetics; Iodide Peroxidase - metabolism; iodides; iodine; Iodine - analysis; Iodine - metabolism; Kelp - chemistry; Kelp - genetics; Kelp - metabolism; Laminaria; Laminaria - chemistry; Laminaria - genetics; Laminaria - metabolism; Laminaria digitata; macroalgae; metabolism; oxidative stress; Plant physiology and development; reactive oxygen species; RESEARCH PAPER; spectroscopy; vanadium; X-radiation; Bromine; Reactive oxygen species; Algae; Marine alga; halocarbons; Antioxidant; Heterokontophyta; In vivo; X ray absorption spectrometry; Botany; Electron paramagnetic resonance; X-ray absorption spectroscopy; Laminaria digitata; brown algae; Speciation; Phaeophyceae; Iodine; electron paramagnetic resonance; reactive oxygen species
• ISSN: 0022-0957; 1460-2431
• DOI: 10.1093/jxb/ert110

The metabolism of bromine in marine brown algae remains poorly understood. This contrasts with the recent finding that the accumulation of iodide in the brown alga Laminaria serves the provision of an inorganic antioxidant – the first case documented from a living system. The aim of this study was to use an interdisciplinary array of techniques to study the chemical speciation, transformation, and function of bromine in Laminaria and to investigate the link between bromine and iodine metabolism, in particular in the antioxidant context. First, bromine and iodine levels in different Laminaria tissues were compared by inductively coupled plasma MS. Using in vivo X-ray absorption spectroscopy, it was found that, similarly to iodine, bromine is predominantly present in this alga in the form of bromide, albeit at lower concentrations, and that it shows similar behaviour upon oxidative stress. However, from a thermodynamic and kinetic standpoint, supported by in vitro and reconstituted in vivo assays, bromide is less suitable than iodide as an antioxidant against most reactive oxygen species except superoxide, possibly explaining why kelps prefer to accumulate iodide. This constitutes the first-ever study exploring the potential antioxidant function of bromide in a living system and other potential physiological roles. Given the tissue-specific differences observed in the content and speciation of bromine, it is concluded that the bromide uptake mechanism is different from the vanadium iodoperoxidase-mediated uptake of iodide in L. digitata and that its function is likely to be complementary to the iodide antioxidant system for detoxifying superoxide.