Microchemical imaging of iodine distribution in the brown alga Laminaria digitata suggests a new mechanism for its accumulation

Abstract

Brown algal kelp species are the most efficient iodine accumulators among all living systems, with an average content of 1.0% of dry weight in Laminaria digitata. The iodine distributions in stipe and blade sections from L. digitata were investigated at tissue and subcellular levels. The quantitative tissue mapping of iodine and other trace elements (Cl, K, Ca, Fe, Zn, As and Br) was provided by the proton microprobe with spatial resolutions down to 2 mum. Chemical imaging at a subcellular resolution (below 100 nm) was performed using the secondary ion mass spectrometry microprobe. Sets of samples were prepared by both chemical fixation and cryofixation procedures. The latter prevented the diffusion and the leaching of labile inorganic iodine species, which were estimated at around 95% of the total content by neutron activation analysis. The distribution of iodine clearly shows a huge, decreasing gradient from the meristoderm to the medulla. The contents of iodine reach very high levels in the more external cell layers, up to 191 +/- 5 mg g(-1) of dry weight in stipe sections. The peripheral tissue is consequently the main storage compartment of iodine. At the subcellular level, iodine is mainly stored in the apoplasm and not in an intracellular compartment as previously proposed. This unexpected distribution may provide an abundant and accessible source of labile iodine species which can be easily remobilized for potential chemical defense and antioxidative activities. According to these imaging data, we proposed new hypotheses for the mechanism of iodine storage in L. digitata tissues.

The time dependence of molecular iodine emission from <i>Laminaria digitata</i>

“…The possibility that the inhomogeneous distribution of I 2 in Laminaria species (Verhaeghe et al, 2008;ArGall et al, 2004;Amat and Srivastava, 1985) could lead to spatial disparities in the I 2 release and hence the occurrence of bursts cannot be determined from these first measurements. Our approach integrates over the entire specimen, therefore even strong spatial differences in the physiological and chemical effectiveness of I 2 release cannot be detected.…”

“…The choice of Laminaria digitata, one of approximately 30 brown algal species (Phaeophyceae) of a genus known as kelp, is due to its high average iodine content of about 1.0% of its dry weight (DW) (Verhaeghe et al, 2008;ArGall et al, 2004;Küpper et al, 1998). Laminaria digitata is characterized by long, leathery laminae (blades) of relatively large size (up to 2 m).…”

Vanadium haloperoxidases: From the discovery 30 years ago to X-ray crystallographic and V K-edge absorption spectroscopic studies

“…One is a VBPO [53], whereas the other isoform is specific for iodide oxidation [54]. No specific iodinated substrate has been yet identified in L. digitata, but this particular VHPO may be involved in the very efficient accumulation of iodide in external tissues of L. digitata [14,74,75]. Another VIPO was recently characterized at the structural level in the marine flavobacterium Z. galactanivorans, which belongs to the bacteroidetes and is associated with both red and brown seaweeds [56].…”

Iodide accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry

“…In addition to iodocarbons, iodine oxide (IO) is also detectable in the atmosphere above kelp beds (9), providing precursors for cloud condensation nuclei (10). Recently, microimaging has revealed that iodine is essentially stored in the extracellular matrix of L. digitata cells located in the peripheral tissues (11). Despite considerable research interest in the role of kelp in the biogeochemical iodine cycle, the identity, speciation, and biological significance of bioaccumulated iodine has remained enigmatic for two centuries.…”

“…Despite considerable research interest in the role of kelp in the biogeochemical iodine cycle, the identity, speciation, and biological significance of bioaccumulated iodine has remained enigmatic for two centuries. In particular, all studies so far have left significant ambiguity as to the chemical speciation of iodine in Laminaria (6,(11)(12)(13)(14)(15)(16)(17)(18)(19)(20).…”