RT Journal Article SR Electronic T1 Snowball Earths, population bottlenecks, and the evolution of marine photosynthetic bacteria JF bioRxiv FD Cold Spring Harbor Laboratory SP 2020.11.24.395392 DO 10.1101/2020.11.24.395392 A1 Hao Zhang A1 Ying Sun A1 Qinglu Zeng A1 Sean A. Crowe A1 Haiwei Luo YR 2021 UL http://biorxiv.org/content/early/2021/03/10/2020.11.24.395392.abstract AB Prochlorococcus are the most abundant photosynthetic organisms in the modern ocean. A massive DNA loss event occurred in their early evolutionary history, leading to highly reduced genomes in nearly all lineages, as well as enhanced efficiency in both nutrient uptake and light absorption. The environmental landscape that shaped this ancient genome reduction, however, remained unknown. Through careful molecular clock analyses, we established that this Prochlorococcus genome reduction occurred during the Neoproterozoic Snowball Earth climate catastrophe. The lethally low temperature and exceedingly dim light during the Snowball Earth event would have inhibited Prochlorococcus growth and proliferation and caused severe population bottlenecks. These bottlenecks are recorded as an excess of deleterious mutations that accumulated across genomic regions in the descendant lineages. Prochlorococcus adaptation to extreme environmental conditions during Snowball Earth intervals can be inferred by tracing the evolutionary paths of genes that encode key metabolic potential. This metabolic potential includes modified lipopolysaccharide structure, strengthened peptidoglycan biosynthesis, the replacement of a sophisticated circadian clock with an hourglass-like mechanism that resets daily for dim light adaption, and the adoption of ammonia diffusion as an efficient membrane transporter-independent mode of nitrogen acquisition. In this way, the Neoproterozoic Snowball Earth event altered the physiological characters of Prochlorococcus, shaping their ecologically vital role as the most abundant primary producers in the modern oceans.Competing Interest StatementThe authors have declared no competing interest.