Genome reduction occurred in earlyProchlorococcuswith an unusually low effective population size

Abstract

AbstractIn the oligotrophic sunlit ocean, the most abundant free-living planktonic bacterial lineages evolve convergently through genome reduction. The cyanobacteriumProchlorococcusresponsible for 10% global oxygen production is a prominent example. The dominant theory known as ‘genome streamlining’ posits that they have extremely large effective population sizes (Ne) such that selection for metabolic efficiency acts to drive genome reduction. Because genome reduction largely took place anciently, this theory builds on the assumption that their ancestors’Newas similarly large. ConstrainingNefor ancient ancestors is challenging because experimental measurements of extinct organisms are impossible and alternatively reconstructing ancestralNewith phylogenetic models gives large uncertainties. Here, we develop a new strategy that leverages agent-based modeling to simulate the change ofNeproxy for ancient ancestors, the genome-wide ratio of radical to conservative nonsynonymous nucleotide substitution rate (dR/dC), in response to the change ofNe. Surprisingly, this proxy shows expected increases with decreases ofNeonly whenNefalls to about 10k – 100k or lower, magnitudes characteristic ofNeof obligate endosymbiont species where drift drives genome reduction. We therefore conclude that drift, rather than selection, is the primary force that droveProchlorococcusgenome reduction.