Molecular and Physiological Acclimation to Low Light and Iron Scarcity in Globally Abundant Oceanic Pelagophyte

Pelagomonas calceolata is a widely distributed marine alga and is among the most numerous eukaryotes on Earth. It is abundant in subsurface chlorophyll maximum layer (SCML) communities where it can be responsible for a majority of nitrate assimilation. Growth in these communities is frequently limited by the lack of iron (Fe), and no eukaryotic phytoplankton species has been shown to require less Fe than P. calceolata. SCML communities are also light limited, resulting in an increased need for Fe-rich photosynthetic proteins. Consequently, to survive and compete in these SCML environments calls for an Fe/light co-limitation specialist. To understand the strategies behind P. calceolata’s success, we profiled this organism’s physiology and gene expression as it experiences Fe/light co-limitation. Our study describes the cellular changes under steady-state Fe limitation and the short-term responses to Fe resupply. Our culture experiments revealed that P. calceolata maintains exceptionally low Fe:C ratios across conditions and dynamically regulates iron-sparing strategies such as flavodoxin expression and substitution of metal-rich proteins. Furthermore, coupling environmental gene expression with culture-based profiles showed that Fe- and light-responsive genes identified in the lab were strongly enriched in SCML metatranscriptomes, indicating that P. calceolata expresses these adaptations in situ. These results demonstrate low Fe tolerance as a key adaptation enabling P. calceolata to thrive in light-limited marine environments and highlight its broader role in oceanic carbon and nitrogen cycling.