Characterization of Iodine-Related Molecular Processes in the Marine Microalga Tisochrysis lutea (Haptophyta)

Abstract

Iodine metabolism is essential for the antioxidant defense of marine algae and in the biogeochemical cycle of iodine. Moreover, some microalgae can synthetize thyroid hormone-like compounds that are essential to sustain food webs. However, knowledge regarding iodine-related molecular processes in microalgae is still scarce. In this study, a de novo transcriptome of Tisochrysis lutea cultured under high iodide concentrations (5 mM) was assembled using both long and short reads. A database termed IsochrysisDB was established to host all genomic information. Gene expression analyses during microalgal growth showed that most of the antioxidant-(aryl, ccp, perox, sod1, sod2, sod3, apx3, ahp1) and iodide-specific deiodinase (dio) genes increased their mRNA abundance progressively until the stationary phase to cope with oxidative stress. Moreover, the increase of dio mRNA abundance in aging cultures indicated that this enzyme was also involved in senescence. Cell treatments with iodide modified the expression of perox whereas treatments with iodate changed the transcript levels of gpx1 and ccp. To test the dependence of perox on iodide, microalgae cells were treated with hydrogen peroxide (H 2 O 2 ) either in presence or absence of iodide observing that several genes related to reactive oxygen species (ROS) deactivation (perox, gpx1, apx2, apx3, ahp1, ahp2, sod1, sod3, and aryl) were transcriptionally activated although with some temporal differences. However, only the expression of perox was dependent on iodide levels indicating this enzyme, acquired by horizontal gene transfer (HGT), could act as a haloperoxidase. All these data indicate that T. lutea activates coordinately the expression of antioxidant genes to cope with oxidative stress. The identification of a phase-regulated deiodinase and a novel haloperoxidase provide new clues about the origin and evolution of thyroid signaling and the antioxidant role of iodine in the marine environment.

Senescence as the main driver of iodide release from a diverse range of marine phytoplankton

“…Studies (Küpper et al, 1997(Küpper et al, , 2008 have suggested that iodate-to-iodide reduction in marine macroalgae is linked to light-induced oxidative stress. Whilst iodide has been shown to control oxidative stress in microalgae (Hernández Javier et al, 2018), a link between iodate reduction and light-induced oxidative stress has yet to be demonstrated in this group of organisms. A better understanding of the purpose and mechanism of iodate-to-iodide reduction in marine phytoplankton would help with the development of process-based models of inorganic iodine cycling in the oceans.…”

“…In addition to uptake the disappearance of iodide may have also indicated conversion into other organic or inorganic forms. Volatile or low-molecular-weight organoiodine compounds are usually found in concentrations in the picomolar range both in monocultures (Hughes et al, 2006) and in the field (Hepach et al, 2016). Dissolved organic iodine (DOI) has been suggested to be a possible intermediate step in the reduction of iodate to iodide.…”

Factors regulating the concentration of particulate iodine in coastal seawater

“…Correspondingly, as described above, it has been reported that the gene expressions of enzymes related to iodine uptake and utilization of thyroxine in phytoplankton are lower in the exponential growth phase than those in the stationary and senescent growth phases (Javier et al, 2018). This suggests that the iodine requirement by phytoplankton is lower in the exponentially growth phase and further potentially indicates that the iodine uptake rate of highly productive phytoplankton is lower than that of steady and senescent phytoplankton.…”

“…As I − is preferentially taken by phytoplankton (de la Cuesta and Manley, 2009), this may indicate enhanced iodine uptake during the senescence. Supplementally, the gene expressions of enzymes related to iodine uptake (peroxidase) and utilization of thyroxine (deiodinase) in phytoplankton reportedly peak at the start of the senescent phase (Javier et al, 2018), potentially indicating that the iodine requirement by phytoplankton increases at this phase. Additionally, HOI produced by phytoplankton from I − (Hill and Manley, 2009) may partially react with detrital organic matter in seawater (Wong, 1982), which potentially leads to the production of particulate organic iodine.…”

Bridging the Gap: Plant‐Endophyte Interactions as a Roadmap to Understanding Small‐Molecule Communication in Marine Microbiomes

“…Marine organisms use an array of halogenases and selectivity for different halogens can be based on electronegativity, ionic radius, reactivity, or natural abundance in the environment . This is particularly relevant to marine organisms that bioaccumulate halogens many hundreds of times higher than their presence in the surrounding seawater . This additionally raises questions about the choice of media for culturing marine organisms, as many marine medias contain significant quantities of bromine but do not have added iodine that mimic levels present in seawater.…”