The smallest phytoplankton species are key actors in oceans biogeochemical cycling and their abundance and distribution are affected with global environmental changes. Among them, algae of the Pelagophyceae class encompass coastal species causative of harmful algal blooms while others are cosmopolitan and abundant. The lack of genomic reference in this lineage is a main limitation to study its ecological importance. Here, we analysed Pelagomonas calceolata relative abundance, ecological niche and potential for the adaptation in all oceans using a complete chromosome-scale assembled genome sequence. Our results show that P. calceolata is one of the most abundant eukaryotic species in the oceans with a relative abundance favoured by high temperature, low-light and iron-poor conditions. Climate change projections based on its relative abundance suggest an extension of the P. calceolata habitat toward the poles at the end of this century. Finally, we observed a specific gene repertoire and expression level variations potentially explaining its ecological success in low-iron and low-nitrate environments. Collectively, these findings reveal the ecological importance of P. calceolata and lay the foundation for a global scale analysis of the adaptation and acclimation strategies of this small phytoplankton in a changing environment.

Eukaryotic phytoplankton are key actors in marine ecosystems, they contribute to atmospheric CO2 sequestration and supply organic matter to the trophic network. Among them, Pelagophytes (Stramenopiles) algae are a diverse class with coastal species causative of harmful algal blooms while others are cosmopolites and abundant in open ocean ecosystems. Despite their ecological importance, only a few genomic references exist limiting our capacity to identify them and study their adaptation mechanisms in a changing environment. Here, we report the complete chromosome-scale assembled genome sequence of Pelagomonas calceolata. We identified unusual large low-GC and gene-rich regions potentially hosting centromeres. These particular genomic structures could be explained by the absence of genes necessary for an important recombination pathway in this species. We identified a large repertoire of genes involved in inorganic nitrogen sensing and uptake as well as many genes replacing iron-required proteins potentially explaining its ecological success in oligotrophic waters. Finally, based on this high-quality assembly, we evaluated P. calceolata relative abundance in all oceans using environmental Tara datasets. Our results suggest that P. calceolata is one of the most abundant eukaryote species in the oceans with a relative abundance driven by the high temperature and iron-poor conditions. Collectively, these findings bring new insights into the biology and ecology of P. calceolata and lay the foundation for the analysis of the adaptation and acclimation strategy of this picophytoplankton.