Prochlorococcus are the smallest and most abundant photosynthetic organisms on Earth, contributing up to 50% of the chlorophyll in the oligotrophic oceans. Despite being important in regulating the carbon cycle in today's ocean, the ecological significance of Prochlorococcus in Earth's history remains elusive. Our new robustly calibrated molecular clock reveals that Prochlorococcus emerged in the deep photic zone of the Tonian oceans. The classical antenna for light harvesting in Cyanobacteria, the phycobilisome, was replaced in Prochlorococcus by the chlorophyll‐based light‐harvesting complex enabling more efficient use of blue light that penetrated to deeper water. Importantly, Prochlorococcus colonization of deep water enhanced access to phosphate, which was rich in upwelled seawater, but likely scarce in the Tonian surface ocean, promoting expansion of Prochlorococcus and associated photosynthetic oxygen production. Colonization of deeper waters would also have improved access to ammonium, leading to the neutral loss of nitrate utilization genes. Our research thus documents the conspicuous emergence of new photosynthetic bacterial lineages in the run-up to the Neoproterozoic oxygenation event, implying an additional layer of eco-evolutionary complexity during this pivotal interval in Earth's history.

Emergence ofProchlorococcusin the Tonian oceans and the initiation of Neoproterozoic oxygenation