Iodide in kelp: an inorganic antioxidant in life impacting atmospheric

chemistry

Frithjof C. Küpper

Biological model: Laminaria digitata (Phaeophyceae)

Courtois, B. (lu par / read by N. Clément), 1813:Découverte d’une substance nouvelle dans le Vareck.Annales de Chimie 88, 304-310

• Iodine as a novel chemical element was discovered in the ashes of Laminaria

Iodine accumulation in Laminaria

• Laminariales (kelps) are a major biogeochemical pump of iodine!

Still unclear:• Chemical form of accumulated iodine? • Biological significance?

• Laminaria is the strongest iodine accumulator in life

The Global Iodine Cycle

euphotic zone

kelp forestsand planktonic algae(accumulation of iodine, iodinated natural products)

IO3-

Nitrate reductase(phytoplankton, bacteria?)

I2, iodocarbons (R-I)(CH2I2, CHI3, CHI3 etc.)

iodine oxide (IO), and: I-, IO3

-, HOI

photolysis

“Iodovolatilisation”

IO provides condensationnuclei for cloud formation

precipitation

terrestrial runoff

diet

Thyroidlactoperoxidase-catalysedincorporation in thyroxine

fossil iodide / iodate deposits

dietarysupple-ments

fertilizers

Millions of years ago

deep waters

sedimentsR-I R + I-

H2S

Bacterial decomposition

IO3-

(predominantly) I-

(release of small amounts from POC)

I2, HOI

+ O2, O3 or H2O2

CH3I

+ organicmatter

I-

Adapted / modified from Feiters, Küpper & Meyer-Klaucke, 2005: J. Synchrotr. Radiation 12, 85-93

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

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.

Iodi

ne c

onte

nt (%

DW

)

0

1

2

3

Winter Spring Summer Autumn

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 Chemistry 13, 257-269.

(stipe section)

25 m

Particle-induced X-ray emissionElemental map of the meristoderm and outer cortes in a L. digitata stipe section

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.

Biological XAS at the EMBL Outstation, Hamburg

e+

synchrotron

whitebeam

Al foilslits 1

slits 2

focussingmirrororder sorting

double crystalmonochromator

(Si 111)

sample

ionizationchambers

I0 It

13 elementfluorescence

detector

calibrator crystal(Si 220) withscintillation

counters

monochromaticbeam

Biological XAS at the EMBL Outstation, Hamburg

Iodine XAS of Laminaria tissues

Iodide (I-) is the accumulated form of iodine in Laminaria!

(Iodine K-edge)

Iodine metabolism and oxidative stress

• Iodine uptake requires low H2O2 levels (< 25 M)

• 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

The oxidative burst in Laminaria• A key element in eukaryotic innate immunity• Triggers in Laminaria: bacterial endotoxins (LPS),

oligoguluronates (oligoalginates)

120 s

123

420 s

123

660 s

123

840 s

123

DCFH-DA : dichlorohydro-fluorescein diacetate

Küpper et al., 2001: Plant Physiology 125, 278-91

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

Cathodic stripping square wave voltammetry (CSSWV)

Strong iodide efflux upon oxidative stress

Oligoguluronate treatment

• No increased levels of oxidized or organic iodine species

Scavenging of ozone (O3) by Laminaria

Laminaria thalli effectively scavenge ozone

When light is present: ultrafine particle formation

Kelp forests contribute to aerosol formation

in the coastal environment

O’Dowd et al., 2002: Nature 417, 632-6

• Iodine oxides as condensation nuclei• “Particle bursts” in the coastal atmosphere

above kelp beds at low tide and high irradiance

Kelp forests contribute to aerosol formation

in the coastal environment

O’Dowd et al., 2002:Nature 417, 632-6

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)

You can smell it!

I2 I2

Taynish National Nature Reserve, Argyll, Scotland, June 8, 2008