Emergence of Prochlorococcus in the Tonian oceans and the initiation of Neoproterozoic oxygenation

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 todays ocean, the ecological significance of Prochlorococcus in Earths history remains elusive. Our new robustly calibrated molecular clock analysis reveals that Prochlorococcus emerged in the deep photic zone of the Tonian (1,000-720 Mya) oceans. The classical light-harvesting antenna complex in Cyanobacteria, i.e., the phycobilisome, was replaced in Prochlorococcus by the chlorophyll{square}based antenna, enabling more efficient use of blue light that penetrates into deeper water. Importantly, Prochlorococcus colonization of deep water enhanced access to phosphate, which was abundant in upwelled seawater, but likely scarce in the Tonian surface ocean, promoting expansion of Prochlorococcus, displacement of incumbent low-light adapted anoxygenic photoferrotrophs, and associated increases in 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 Earths history.