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

Frithjof C Kuepper, Lucy J Carpenter, Catherine Leblanc, Chiaki Toyama, Yuka Uchida, Benjamin H Maskrey, Joanne Robinson, Elodie F Verhaeghe, Gill Malin, George W Luther, Peter M H Kroneck, Bernard Kloareg, Wolfram Meyer-Klaucke, Yasuyuki Muramatsu, Ian L Megson, Philippe Potin, Martin C Feiters

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Abstract

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.
Original languageEnglish
Pages (from-to)2653-2664
Number of pages12
JournalJournal of Experimental Botany
Volume64
Issue number10
DOIs
Publication statusPublished - Jul 2013

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Laminaria
bromine
Bromine
iodine
Iodine
Iodides
iodides
Antioxidants
bromides
Bromides
antioxidants
Phaeophyta
Phaeophyceae
algae
Superoxides
superoxide anion
X-Ray Absorption Spectroscopy
uptake mechanisms
vanadium
chemical speciation

Keywords

  • antioxidant
  • brown algae
  • electron paramagnetic resonance
  • halocarbons
  • reactive oxygen species
  • x-ray absorption spectroscopy

Cite this

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

In: Journal of Experimental Botany, Vol. 64, No. 10, 07.2013, p. 2653-2664.

Research output: Contribution to journalArticle

Kuepper, FC, Carpenter, LJ, Leblanc, C, Toyama, C, Uchida, Y, Maskrey, BH, Robinson, J, Verhaeghe, EF, Malin, G, Luther, GW, Kroneck, PMH, Kloareg, B, Meyer-Klaucke, W, Muramatsu, Y, Megson, IL, Potin, P & Feiters, MC 2013, 'In vivo speciation studies and antioxidant properties of bromine in Laminaria digitata reinforce the significance of iodine accumulation for kelps', Journal of Experimental Botany, vol. 64, no. 10, pp. 2653-2664. https://doi.org/10.1093/jxb/ert110
Kuepper, 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. / In vivo speciation studies and antioxidant properties of bromine in Laminaria digitata reinforce the significance of iodine accumulation for kelps. In: Journal of Experimental Botany. 2013 ; Vol. 64, No. 10. pp. 2653-2664.
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abstract = "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.",
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AU - Toyama, Chiaki

AU - Uchida, Yuka

AU - Maskrey, Benjamin H

AU - Robinson, Joanne

AU - Verhaeghe, Elodie F

AU - Malin, Gill

AU - Luther, George W

AU - Kroneck, Peter M H

AU - Kloareg, Bernard

AU - Meyer-Klaucke, Wolfram

AU - Muramatsu, Yasuyuki

AU - Megson, Ian L

AU - Potin, Philippe

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N2 - 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.

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