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Research Article

Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry

Frithjof C. Küpper, Lucy J. Carpenter, Gordon B. McFiggans, Carl J. Palmer, Tim J. Waite, Eva-Maria Boneberg, Sonja Woitsch, Markus Weiller, Rafael Abela, Daniel Grolimund, Philippe Potin, Alison Butler, George W. Luther III, Peter M. H. Kroneck, Wolfram Meyer-Klaucke, and Martin C. Feiters
  1. aScottish Association for Marine Science, Dunstaffnage Marine Laboratory, Oban, Argyll PA37 1QA, Scotland, United Kingdom;
  2. bFachbereich Biologie, Universität Konstanz, D-78457 Konstanz, Germany;
  3. cDepartment of Chemistry and Biochemistry, University of California, Santa Barbara, CA 93106;
  4. eDepartment of Chemistry, University of York, York YO10 5DD, United Kingdom;
  5. fSchool of Earth, Atmospheric, and Environmental Sciences, University of Manchester, Manchester M13 9PL, United Kingdom;
  6. hCollege of Marine Studies, University of Delaware, Lewes, DE 19958;
  7. iBiotechnologie Institut Thurgau, Unterseestrasse 47, CH-8280 Kreuzlingen, Switzerland;
  8. jSwiss Light Source, Paul Scherrer Institute, CH-5232 Villigen, Switzerland;
  9. kCentre National de la Recherche Scientifique and Université Pierre et Marie Curie Paris–VI, Station Biologique de Roscoff, Place Georges Teissier, BP 74, F-29682 Roscoff cedex, Bretagne, France;
  10. lEuropean Molecular Biology Laboratory, Hamburg Unit, Deutsches Elektronen Synchrotron, Notkestrasse 85, D-22607 Hamburg, Germany; and
  11. mDepartment of Organic Chemistry, Institute of Molecules and Materials, Radboud University Nijmegen, 1 Toernooiveld, NL-6525 ED, Nijmegen, The Netherlands

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PNAS May 13, 2008 105 (19) 6954-6958; https://doi.org/10.1073/pnas.0709959105
Frithjof C. Küpper
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  • For correspondence: fck@sams.ac.uk
Lucy J. Carpenter
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Gordon B. McFiggans
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Carl J. Palmer
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Tim J. Waite
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Eva-Maria Boneberg
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Sonja Woitsch
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Markus Weiller
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Rafael Abela
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Daniel Grolimund
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Philippe Potin
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Alison Butler
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George W. Luther III
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Peter M. H. Kroneck
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Wolfram Meyer-Klaucke
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Martin C. Feiters
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  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved March 11, 2008 (received for review October 18, 2007)

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Abstract

Brown algae of the Laminariales (kelps) are the strongest accumulators of iodine among living organisms. They represent a major pump in the global biogeochemical cycle of iodine and, in particular, the major source of iodocarbons in the coastal atmosphere. Nevertheless, the chemical state and biological significance of accumulated iodine have remained unknown to this date. Using x-ray absorption spectroscopy, we show that the accumulated form is iodide, which readily scavenges a variety of reactive oxygen species (ROS). We propose here that its biological role is that of an inorganic antioxidant, the first to be described in a living system. Upon oxidative stress, iodide is effluxed. On the thallus surface and in the apoplast, iodide detoxifies both aqueous oxidants and ozone, the latter resulting in the release of high levels of molecular iodine and the consequent formation of hygroscopic iodine oxides leading to particles, which are precursors to cloud condensation nuclei. In a complementary set of experiments using a heterologous system, iodide was found to effectively scavenge ROS in human blood cells.

  • algae
  • Laminaria
  • x-ray absorption spectroscopy
  • cathodic stripping square wave voltammetry

Footnotes

  • dTo whom correspondence should be addressed. E-mail: fck{at}sams.ac.uk
  • ↵gPresent address: Department of Oceanography, University of Cape Town, Rondebosch 7701, South Africa.

  • Author contributions: F.C.K., L.J.C., G.B.M., P.P., A.B., G.W.L., P.M.H.K., W.M.-K., and M.C.F. designed research; F.C.K., L.J.C., G.B.M., C.J.P., T.J.W., E.-M.B., S.W., M.W., R.A., D.G., P.P., G.W.L., W.M.-K., and M.C.F. performed research; L.J.C., T.J.W., G.W.L., W.M.-K., and M.C.F. contributed new reagents/analytic tools; F.C.K., L.J.C., G.B.M., C.J.P., T.J.W., E.-M.B., S.W., M.W., R.A., D.G., P.P., G.W.L., W.M.-K., and M.C.F. analyzed data; and F.C.K., L.J.C., G.B.M., P.P., A.B., G.W.L., P.M.H.K., W.M.-K., and M.C.F. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0709959105/DCSupplemental.

  • © 2008 by The National Academy of Sciences of the USA
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Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry
Frithjof C. Küpper, Lucy J. Carpenter, Gordon B. McFiggans, Carl J. Palmer, Tim J. Waite, Eva-Maria Boneberg, Sonja Woitsch, Markus Weiller, Rafael Abela, Daniel Grolimund, Philippe Potin, Alison Butler, George W. Luther, Peter M. H. Kroneck, Wolfram Meyer-Klaucke, Martin C. Feiters
Proceedings of the National Academy of Sciences May 2008, 105 (19) 6954-6958; DOI: 10.1073/pnas.0709959105

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Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry
Frithjof C. Küpper, Lucy J. Carpenter, Gordon B. McFiggans, Carl J. Palmer, Tim J. Waite, Eva-Maria Boneberg, Sonja Woitsch, Markus Weiller, Rafael Abela, Daniel Grolimund, Philippe Potin, Alison Butler, George W. Luther, Peter M. H. Kroneck, Wolfram Meyer-Klaucke, Martin C. Feiters
Proceedings of the National Academy of Sciences May 2008, 105 (19) 6954-6958; DOI: 10.1073/pnas.0709959105
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