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Iodide Accumulation Provides Kelp with an Inorganic Antioxidant Impacting Atmospheric Chemistry

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Iodide Accumulation Provides Kelp with an Inorganic Antioxidant Impacting Atmospheric Chemistry Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry Frithjof C. Ku¨ ppera,b,c,d, Lucy J. Carpentere, Gordon B. McFiggansf, Carl J. Palmere,g, Tim J. Waiteh, Eva-Maria Bonebergb,i, Sonja Woitschb, Markus Weillerb, Rafael Abelaj, Daniel Grolimundj, Philippe Potink, Alison Butlerc, George W. Luther IIIh, Peter M. H. Kroneckb, Wolfram Meyer-Klauckel, and Martin C. Feitersm aScottish Association for Marine Science, Dunstaffnage Marine Laboratory, Oban, Argyll PA37 1QA, Scotland, United Kingdom; bFachbereich Biologie, Universita¨t Konstanz, D-78457 Konstanz, Germany; cDepartment of Chemistry and Biochemistry, University of California, Santa Barbara, CA 93106; eDepartment of Chemistry, University of York, York YO10 5DD, United Kingdom; fSchool of Earth, Atmospheric, and Environmental Sciences, University of Manchester, Manchester M13 9PL, United Kingdom; hCollege of Marine Studies, University of Delaware, Lewes, DE 19958; iBiotechnologie Institut Thurgau, Unterseestrasse 47, CH-8280 Kreuzlingen, Switzerland; jSwiss Light Source, Paul Scherrer Institute, CH-5232 Villigen, Switzerland; 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; lEuropean Molecular Biology Laboratory, Hamburg Unit, Deutsches Elektronen Synchrotron, Notkestrasse 85, D-22607 Hamburg, Germany; and mDepartment of Organic Chemistry, Institute of Molecules and Materials, Radboud University Nijmegen, 1 Toernooiveld, NL-6525 ED, Nijmegen, The Netherlands Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved March 11, 2008 (received for review October 18, 2007) Brown algae of the Laminariales (kelps) are the strongest accumu- In this study, we first address the unresolved question of the lators of iodine among living organisms. They represent a major chemical state of iodine in Laminaria under different physio- pump in the global biogeochemical cycle of iodine and, in partic- logical conditions, using x-ray absorption spectroscopy (XAS) as ular, the major source of iodocarbons in the coastal atmosphere. a noninvasive probe, and show that the only detectable form of Nevertheless, the chemical state and biological significance of iodine is iodide ion. This is not hydrated as in an aqueous accumulated iodine have remained unknown to this date. Using solution of sodium iodide but instead has its hydration shell x-ray absorption spectroscopy, we show that the accumulated disrupted by interactions with organic molecules with which it is form is iodide, which readily scavenges a variety of reactive oxygen associated. Upon oxidative stress, high levels of iodide are species (ROS). We propose here that its biological role is that of an released and are detectable in the surrounding seawater by inorganic antioxidant, the first to be described in a living system. voltammetric methods. Using an array of gas chromatography– Upon oxidative stress, iodide is effluxed. On the thallus surface and mass spectrometry (GC-MS), aerosol particle counting, and in the apoplast, iodide detoxifies both aqueous oxidants and spectrophotometry to assess both organic and inorganic iodine ozone, the latter resulting in the release of high levels of molecular emissions into the gas phase, we demonstrate that on the thallus iodine and the consequent formation of hygroscopic iodine oxides surface and in the apoplast, iodide detoxifies both aqueous leading to particles, which are precursors to cloud condensation oxidants and ozone, the latter resulting in the release of molec- nuclei. In a complementary set of experiments using a heterolo- ular iodine and the concomitant, consequent formation of gous system, iodide was found to effectively scavenge ROS in particles, which can act as cloud condensation nuclei. We human blood cells. propose that iodide in kelp constitutes an extracellular protec- tion against oxidative stress and the first identified inorganic algae ͉ Laminaria ͉ x-ray absorption spectroscopy ͉ antioxidant in a living system. cathodic stripping square wave voltammetry Results and Discussion The known reactivity of many iodine species and a hypothesis from he element iodine was first isolated from kelp ashes two the biomedical field (7) led us to investigate its chemical identity in Tcenturies ago by Courtois in the context of the search for raw kelp with a noninvasive technique, x-ray absorption spectroscopy materials for explosives (chiefly potassium nitrate) during the (XAS) (21). The iodine K-edge XAS of freshly frozen L. digitata Napoleonic Wars (1, 2). Brown algal kelp species such as thalli showed a featureless edge (Fig. 1a) and weak EXAFS Laminaria digitata are the most effective known living iodine oscillations [supporting information (SI) Fig. S1]. The correspond- accumulators, with tissue concentrations often exceeding 50 mM ing Fourier transform (FT) (Fig. 1b) exhibited no peaks below 3 Å, (3). Until the large-scale exploitation of brine waters accompa- indicating the absence of covalent bonds to iodine, which is nying natural gas deposits for the recovery of iodine salts (4, 5), supported by L3-edge measurements (SI Text and Fig. S2). We Laminariales remained a major commercial source of iodine (6). conclude that iodine is accumulated in Laminaria in its reduced The importance of iodine for thyroid function is paramount (7). form, iodide. Moreover, the strongest FT peak is at the same Long before the discovery of this element, the beneficial effect distance, Ϸ3.5 Å, as for hydrated iodide in NaI solution (22), where of iodine-rich seaweeds in treating goiter had been recognized initially in China and later in medieval Europe (2). In coastal regions, Laminariales are a major contributor to the iodine flux 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. from the ocean to the atmosphere through the production of 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. volatile halocarbons (8). In addition to iodocarbons, iodine oxide 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., (IO) is also detectable in the atmosphere above kelp beds (9), 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., providing precursors for cloud condensation nuclei (10). Re- P.P., A.B., G.W.L., P.M.H.K., W.M.-K., and M.C.F. wrote the paper. cently, microimaging has revealed that iodine is essentially stored The authors declare no conflict of interest. in the extracellular matrix of L. digitata cells located in the This article is a PNAS Direct Submission. peripheral tissues (11). Despite considerable research interest in dTo whom correspondence should be addressed. E-mail: [email protected]. the role of kelp in the biogeochemical iodine cycle, the identity, gPresent address: Department of Oceanography, University of Cape Town, Rondebosch speciation, and biological significance of bioaccumulated iodine 7701, South Africa. has remained enigmatic for two centuries. In particular, all This article contains supporting information online at www.pnas.org/cgi/content/full/ studies so far have left significant ambiguity as to the chemical 0709959105/DCSupplemental. speciation of iodine in Laminaria (6, 11–20). © 2008 by The National Academy of Sciences of the USA 6954–6958 ͉ PNAS ͉ May 13, 2008 ͉ vol. 105 ͉ no. 19 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0709959105 Downloaded by guest on September 29, 2021 a b Fig. 1. XAS of L. digitata tissues, including time course of experiment with fresh Laminaria thalli stressed with oligoguluronates (GG). (a) Iodine XAS (K-edge region). (b) Phase-corrected FT of k3-weighted EXAFS (cf. Fig. S1). Solid lines, experimental; dashed lines, simulations. (Inset) Schematic representation of a Ϫ cross-section of the immediate environment of the I ion, showing the change in the solvation by many hydrogen-bonded H2O molecules in 20 mM NaI solution (Upper) to association by fewer hydrogen bonds to biomolecules in fresh Laminaria (Lower; examples clockwise from top left are polyphenol, peptide, and carbohydrate). In Laminaria tissues, iodine is overwhelmingly stored as iodide. In fresh, live tissues, iodide is largely present in association with biomolecules including polyols (e.g., carbohydrates), phenols (e.g., phlorotannins), and amides (e.g., proteins), replacing the highly ordered hydration shell. Upon oxidative stress, part of this iodide is mobilized, as reflected in a more ordered hydration shell. When freeze-dried tissues are exposed to 2 mM hydrogen peroxidein seawater (simulating local concentrations observed during an oxidative burst), much of the available iodine is incorporated into aromatic organic molecules as reflected by the strong change in the EXAFS spectrum (highlighted by the vertical lines at 33,219 eV and 33,266 eV, respectively). Black, lyophilized Laminaria 2 2 2 rehydrated in seawater with 2 mM H2O2 [simulation: 1.0 phenyl at 2.1 Å, a ϭ 0.003 Å (a, Debye–Waller-type factor as 2␴ in Å )]; pink, lyophilized Laminaria (2.2 O at 3.51 Å, a ϭ 0.038 Å2); red, fresh Laminaria (1.6 O at 3.58 Å, a ϭ 0.005 Å2); sea green, 20 min after exposure to GG (2.8 O at 3.58 Å, a ϭ 0.021 Å2); blue, 3 h after exposure to GG (3.9 O at 3.56 Å, a ϭ 0.038 Å2); plum, 20 mM NaI (10.0 O at 3.56 Å, a ϭ 0.034 Å2). A complete list of all simulation parameters with fitting errors is available as Table S1. this peak represents oxygen atoms of the solvent, water.
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