LAUSR

Significance The marine unicellular cyanobacterium Prochlorococcus is the most abundant photosynthetic organism on Earth. Members of this genus are classically thought to be adapted to high-oxygen and nutrient-poor ocean conditions, with a principle divergence between high-light and low-light ecotypes. We show that the most basal Prochlorococcus lineages are adapted to the low-oxygen, low-light, and high-nutrient conditions found in the dimly illuminated waters of anoxic marine zones. The most basal lineages have retained phycobilisomes as light-harvesting antennae—a characteristic of most other cyanobacteria—whose loss was thought to define all Prochlorococcus. As oxygenic photosynthesis drove ocean oxidation in the ancient Earth, oxygen appears to have played as much a role as light and nutrients in driving Prochlorococcus evolution. Marine picocyanobacteria of the genus Prochlorococcus are the most abundant photosynthetic organisms in the modern ocean, where they exert a profound influence on elemental cycling and energy flow. The use of transmembrane chlorophyll complexes instead of phycobilisomes as light-harvesting antennae is considered a defining attribute of Prochlorococcus. Its ecology and evolution are understood in terms of light, temperature, and nutrients. Here, we report single-cell genomic information on previously uncharacterized phylogenetic lineages of this genus from nutrient-rich anoxic waters of the eastern tropical North and South Pacific Ocean. The most basal lineages exhibit optical and genotypic properties of phycobilisome-containing cyanobacteria, indicating that the characteristic light-harvesting antenna of the group is not an ancestral attribute. Additionally, we found that all the indigenous lineages analyzed encode genes for pigment biosynthesis under oxygen-limited conditions, a trait shared with other freshwater and coastal marine cyanobacteria. Our findings thus suggest that Prochlorococcus diverged from other cyanobacteria under low-oxygen conditions before transitioning from phycobilisomes to transmembrane chlorophyll complexes and may have contributed to the oxidation of the ancient ocean.