Diatoms are a key taxon of eukaryotic phytoplankton and a major contributor to global carbon fixation. They are ubiquitous in the marine ecosystem despite marked gradients in environmental properties, such as dissolved iron concentrations, between coastal and oceanic waters. Previous studies have shown that offshore species of diatoms and other eukaryotic algae have evolved lower iron requirements to subsist in iron-poor oceanic waters, but the biochemical mechanisms responsible for their decreased iron demand are unknown. Here we show, using laboratory-cultured model species, a fundamental difference between a coastal and an oceanic diatom in their photosynthetic architecture. Specifically, the oceanic diatom had up to fivefold lower photosystem I and up to sevenfold lower cytochrome b6f complex concentrations than a coastal diatom. These changes to the photosynthetic apparatus markedly decrease the cellular iron requirements of the oceanic diatom but not its photosynthetic rates. However, oceanic diatoms might have also sacrificed their ability to acclimate to rapid fluctuations in light intensity--a characteristic of dynamic and turbid coastal waters. We suggest that diatoms, and probably other eukaryotic algal taxa, exploited this difference in the underwater light climate between oceanic and coastal waters, enabling them to decrease their iron requirements without compromising photosynthetic capacity. This adaptation probably facilitated the colonization of the open ocean by diatoms, and contributes to their persistence in this iron-impoverished environment.