Genome reduction occurred in early Prochlorococcus with an unusually low effective population size

Abstract

In the oligotrophic sunlit ocean, the most abundant free-living planktonic bacterial lineages evolve convergently through genome reduction. The cyanobacterium Prochlorococcus responsible 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 Ne was similarly large. Constraining Ne for ancient ancestors is challenging because experimental measurements of extinct organisms are impossible and alternatively reconstructing ancestral Ne with phylogenetic models gives large uncertainties. Here, we develop a new strategy that leverages agent-based modeling to simulate the change of Ne proxy for ancient ancestors, the genome-wide ratio of radical to conservative nonsynonymous nucleotide substitution rate (dR/dC), in response to the change of Ne. Surprisingly, this proxy shows expected increases with decreases of Ne only when Ne falls to about 10k - 100k or lower, magnitudes characteristic of Ne of obligate endosymbiont species where drift drives genome reduction. We therefore conclude that drift, rather than selection, is the primary force that drove Prochlorococcus genome reduction.