Sunlight is the ultimate source of energy for almost all organisms. The conversion of light energy into chemical energy (phototrophy) is powered by two mechanistically distinct processes, employing chlorophyll-containing photochemical reaction centres and membrane-embedded rhodopsin photoreceptors. Rhodopsins powering phototrophy in prokaryotes were recently also discovered in eukaryotic marine phytoplankton, including the diatom Fragilariopsis cylindrus. Homologous sequences were found abundant in a global metatranscriptome survey of marine eukaryotic phytoplankton, indicating their ecological importance. Functional analysis using two-electron voltage clamp in combination with the Xenopus laevis oocyte expression system provided direct experimental evidence for light-dependent proton pumping. Additionally, absolute gene expression analysis using RT-qPCR showed highest transcript abundances in iron-limited cultures and the analysis of rhodopsin transcript abundances in eukaryotic metatranscriptomes showed significant correlations (R2=0.917) with dissolved iron concentrations in ocean surface waters. Furthermore, transgenic diatoms complemented with Fragilariopsis rhodopsin showed enhanced growth during iron limitation. Together, these data provide strong evidence for the global significance of rhodopsins from eukaryotic marine phytoplankton in iron-limited areas of the ocean by providing a trace metal-independent mechanism to photosynthesis.

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