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Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation

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Abstract

Brown algal kelp species are the most efficient iodine accumulators among all living systems, with an average content of 1.0% of dry weight in Laminaria digitata. The iodine distributions in stipe and blade sections from L. digitata were investigated at tissue and subcellular levels. The quantitative tissue mapping of iodine and other trace elements (Cl, K, Ca, Fe, Zn, As and Br) was provided by the proton microprobe with spatial resolutions down to 2 μm. Chemical imaging at a subcellular resolution (below 100 nm) was performed using the secondary ion mass spectrometry microprobe. Sets of samples were prepared by both chemical fixation and cryofixation procedures. The latter prevented the diffusion and the leaching of labile inorganic iodine species, which were estimated at around 95% of the total content by neutron activation analysis. The distribution of iodine clearly shows a huge, decreasing gradient from the meristoderm to the medulla. The contents of iodine reach very high levels in the more external cell layers, up to 191 ± 5 mg g−1 of dry weight in stipe sections. The peripheral tissue is consequently the main storage compartment of iodine. At the subcellular level, iodine is mainly stored in the apoplasm and not in an intracellular compartment as previously proposed. This unexpected distribution may provide an abundant and accessible source of labile iodine species which can be easily remobilized for potential chemical defense and antioxidative activities. According to these imaging data, we proposed new hypotheses for the mechanism of iodine storage in L. digitata tissues.

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Abbreviations

LOD:

Limit of detection

NAA:

Neutron activation analysis

PIXE:

Particle-induced X-ray emission

RBS:

Rutherford backscattering spectrometry

SIMS:

Secondary ion mass spectrometry

vHPO:

Vanadium-dependent haloperoxidase

VIOCs:

Volatile iodinated organic compounds

vIPO:

Vanadium-dependent iodoperoxidase

XAS:

X-ray absorption spectroscopy

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Acknowledgements

This study was supported by a grant from the national program Toxicologie Nucléaire Environnementale (TOXNUC-E) and by CEA and CNRS. We are also grateful to CEA and the TOXNUC-E program for PhD fellowships to E.F.V. and A.F.

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Authors and Affiliations

  1. iBiTec-S, Service de Chimie Bioorganique et de Marquage, CEA Saclay, Bât. 547, 91191, Gif-sur-Yvette Cedex, France

    Elodie Françoise Verhaeghe, Charles Mioskowski & Yves Ambroise

  2. UMR7139, Marine Plants and Biomolecules, Laboratoire International Associé, Dispersal and Adaptation in Marine Species, Station Biologique, Université Pierre et Marie Curie-Paris 6/CNRS, 29682, Roscoff Cedex, France

    Catherine Leblanc & Philippe Potin

  3. CNRS/Université Bordeaux 1, Groupe d’Imagerie Chimique Cellulaire et Spéciation, CNAB UMR 5084, BP 120 Le Haut-Vigneau, 33175, Gradignan Cedex, France

    Aurélien Fraysse, Guillaume Devès & Richard Ortega

  4. Laboratoire de Microscopie Ionique, Institut Curie, 91405, Orsay, France

    Jean-Luc Guerquin-Kern & Ting-Di Wu

  5. INSERM U759, 91405, Orsay, France

    Jean-Luc Guerquin-Kern & Ting-Di Wu

Authors
  1. Elodie Françoise Verhaeghe
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  2. Aurélien Fraysse
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  3. Jean-Luc Guerquin-Kern
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  4. Ting-Di Wu
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  5. Guillaume Devès
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  6. Charles Mioskowski
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  7. Catherine Leblanc
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  8. Richard Ortega
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  9. Yves Ambroise
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  10. Philippe Potin
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Corresponding authors

Correspondence to Elodie Françoise Verhaeghe or Philippe Potin.

Additional information

In memory of Dr. Charles Mioskowski, “Miko,” who died on 2 June 2007.

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Verhaeghe, E.F., Fraysse, A., Guerquin-Kern, JL. et al. Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. J Biol Inorg Chem 13, 257–269 (2008). https://doi.org/10.1007/s00775-007-0319-6

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  • DOI: https://doi.org/10.1007/s00775-007-0319-6

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