Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry

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.

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 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 peroxide in 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 rehydrated in seawater with 2 mM H₂O₂ [simulation: 1.0 phenyl at 2.1 Å, a = 0.003 Ų (a, Debye–Waller-type factor as 2σ² in Ų)]; pink, lyophilized Laminaria (2.2 O at 3.51 Å, a = 0.038 Ų); red, fresh Laminaria (1.6 O at 3.58 Å, a = 0.005 Ų); sea green, 20 min after exposure to GG (2.8 O at 3.58 Å, a = 0.021 Ų); blue, 3 h after exposure to GG (3.9 O at 3.56 Å, a = 0.038 Ų); plum, 20 mM NaI (10.0 O at 3.56 Å, a = 0.034 Ų). A complete list of all simulation parameters with fitting errors is available as Table S1.

Fig. 2.

Time course of iodide efflux during an oligoguluronate-triggered oxidative burst (control, diamonds; GG treatment, squares). The arrow highlights the addition of 100 μg·ml⁻¹ GG, triggering an oxidative burst. At the indicated times, external medium aliquots were taken, and iodide was determined voltammetrically. The data are representative of five experiments.

Fig. 3.

Scavenging of ozone by Laminaria. (a) Concentrations of O₃ in a 2 liter·min⁻¹ flow of zero air (i.e., particle-free, scrubbed) measured before (diamonds) and after (triangles) a glass chamber containing ≈5 g FW (surface area ≈100 cm²) Laminaria. A range of different O₃ concentrations were applied over the course of one experiment, starting with high concentrations that were reduced in steps. Switching the O₃ measurement flow from before to after the chamber or vice versa necessitated temporarily disturbing the total flow, hence the several minutes taken for the O₃ levels to stabilize. Measurements made before the chamber are shown as filled symbols, and those made after the chamber are shown as open symbols. Experiments with an empty chamber show <8% steady-state loss of O₃ to chamber walls. (b) Rate of ozone loss over ≈100-cm² strips of L. digitata in the flow chamber. The data are representative of 14 independent experiments. For comparison, typical O₃ concentrations in the marine boundary layer are of the order of a few tens of parts per billion.

Fig. 4.

A model of iodine metabolism in Laminaria. Laminaria, when submerged and unstressed (a), accumulates iodide from seawater mediated by vanadium haloperoxidase (turquoise). In the tissues and as shown in this study, I⁻ is the accumulated form. When oxidative stress occurs (red), iodide is released to detoxify ROS in the apoplast at the thallus surface outside of the cell membrane, including both aqueous (e.g., H₂O₂) and gaseous (O₃) oxidants. ROS scavenging reactions in the aqueous phase such as halide-assisted disproportionation of H₂O₂ will result in the regeneration of iodide in a cyclic reaction sequence. (a) During oxidative stress at high tide (e.g., due to an oxidative burst caused by alginate-degrading bacteria in a biofilm), iodide is released into the surrounding seawater. (b) In contrast, aerosol particle bursts result mainly from molecular iodine released directly from Laminaria into the coastal atmosphere, as a consequence of the ozone-scavenging reactivity of iodide on kelp surfaces at low tide.