Iodide in kelp: an inorganic antioxidant in life impacting atmospheric chemistry

1. Iodide in kelp: an inorganic antioxidant in life impacting atmospheric chemistry Frithjof C. Küpper

2. Biological model: Laminaria digitata (Phaeophyceae)

3. Iodine as a novel chemical element was discovered in the ashes of Laminaria Courtois, B. (lu par / read by N. Clément), 1813: Découverte d’une substance nouvelle dans le Vareck. Annales de Chimie 88, 304-310

4. Iodine accumulation in Laminaria • Laminariales (kelps) are a major biogeochemical pump of iodine! • Laminaria is the strongest iodine accumulator in life Still unclear: • Chemical form of accumulated iodine? • Biological significance?

5. The Global Iodine Cycle iodine oxide (IO),and: I-, IO3-, HOI Thyroidlactoperoxidase-catalysedincorporation in thyroxine IO provides condensationnuclei for cloud formation photolysis precipitation I2, iodocarbons (R-I) (CH2I2, CHI3, CHI3 etc.) diet CH3I “Iodovolatilisation” fertilizers dietarysupple-ments kelp forests and planktonic algae (accumulation of iodine, iodinated natural products) euphotic zone + organicmatter Nitrate reductase (phytoplankton, bacteria?) I2, HOI IO3- I- terrestrial runoff + O2, O3 or H2O2 deep waters IO3-(predominantly) I-(release of small amounts from POC) fossil iodide / iodate deposits H2S Bacterial decomposition Millions of years ago R-I R + I- sediments Adapted / modified from Feiters, Küpper & Meyer-Klaucke, 2005: J. Synchrotr. Radiation 12, 85-93

6. Iodine accumulation in Laminaria • Requirement of an intact cell wall (apoplast) • Role of hydrogen peroxide and haloperoxidases in iodine uptake • Iodine efflux upon oxidative stress Küpper, F.C.; Schweigert, N.; ArGall, E.; Legendre, J.M.; Vilter, H.; Kloareg, B., 1998: Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta 207, 163-171

7. 3 2 Iodine content (% DW) 1 0 Winter Spring Summer Autumn Iodine accumulation in Laminaria • Strong seasonality! ArGall, E.; Küpper, F.C.; Kloareg, B., 2004: A survey of iodine contents in Laminaria digitata. Botanica Marina 47, 30-37.

8. Particle-induced X-ray emission Elemental map of the meristoderm and outer cortes in a L. digitata stipe section (stipe section) 25 mm Iodine accumulation in Laminaria • Accumulation in cortical tissues Verhaeghe, E.F.; Fraysse, A.; Guerquin-Kern, J.-L.; Wu, T.-D.; Devès, G.; Mioskowski, C.; Leblanc, C.; Ortega, R.; Ambroise, Y.; Potin, P., 2008:Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation. Journal of Biological Inorganic Chemistry13, 257-269.

9. Iodine accumulation in Laminaria Techniques used in this study: • GC/MS • Gas-phase particle counters • Cathodic stripping square wave voltammetry (CSSWV) • X-ray absorption spectroscopy using synchrotron radiation (XAS) etc.

10. Biological XAS at the EMBL Outstation, Hamburg

11. Biological XAS at the EMBL Outstation, Hamburg

12. Iodine XAS of Laminaria tissues (Iodine K-edge) • Iodide (I-) is the accumulated form of iodine in Laminaria!

13. Iodine metabolism and oxidative stress • Iodine uptake requires low H2O2 levels (< 25 mM) • Higher concentrations of H2O2 result in iodine efflux Oxidative stress in Laminaria: • Oxidative (respiratory) burst – a defense reaction • Desiccation, high temperatures, high irradiance and exposure to atmospheric oxidants at low tide

14. 1 2 3 1 2 3 120 s 420 s 1 2 3 1 2 3 840 s 660 s The oxidative burst in Laminaria • A key element in eukaryotic innate immunity • Triggers in Laminaria: bacterial endotoxins (LPS), oligoguluronates (oligoalginates) DCFH-DA : dichlorohydro-fluorescein diacetate Küpper et al., 2001: Plant Physiology 125, 278-91

15. Monitoring the iodine pool during the oxidative burst in Laminaria with XAS • EXAFS: Oxidative stress results in a change of the solution environment of accumulated iodide (towards an aqueous, hydrated form) • XANES: No changes in the redox state of iodine – only iodide is detectable

16. Cathodic stripping square wave voltammetry (CSSWV) Oligoguluronate treatment • Strong iodide efflux upon oxidative stress • No increased levels of oxidized or organic iodine species

17. Scavenging of ozone (O3) by Laminaria • Laminaria thalli effectively scavenge ozone • When light is present: ultrafine particle formation

18. Kelp forests contribute to aerosol formation in the coastal environment • Iodine oxides as condensation nuclei • “Particle bursts” in the coastal atmosphere above kelp beds at low tide and high irradiance O’Dowd et al., 2002: Nature 417, 632-6

19. Kelp forests contribute to aerosol formation in the coastal environment O’Dowd et al., 2002:Nature 417, 632-6

20. Kelp iodine emissions into the coastal atmosphere • “Iodovolatilisation” discovered in 1920s by Kylin and Dangeard: I2 detected with starch paper • J. Lovelock, 1973: Discovery of methyl iodide emissions from seaweeds • B. Alicke et al., 1999: High IO levels above kelp beds at low tide • L.J. Carpenter et al., 2000: CH2I2 main species emitted by Laminaria (total iodine emissions: 0.09 – 0.5 pmol g FW-1 min-1) • This study: High I2 fluxes due to reaction of O3 with I- on seaweed surface (130 pmol g FW-1 min-1)

21. I2 I2 You can smell it! Taynish National Nature Reserve, Argyll, Scotland, June 8, 2008