Environmental Sequence Data from the Sargasso Sea Reveal That the Characteristics of Genome Reduction in Prochlorococcus Are Not a Harbinger for an Escalation in Genetic Drift

The marine cyanobacterium Prochlorococcus MED4 has the smallest sequenced genome of any photosynthetic organism. Prochlorococcus MED4 shares many genomic characteristics with chloroplasts and bacterial endosymbionts, including a reduced coding capacity, missing DNA repair genes, a minimal transcriptional regulatory network, a marked AT% bias, and an accelerated rate of amino acid changes. In chloroplasts and endosymbionts, these molecular phenotypes appear to be symptomatic of a relative increase in genetic drift due to restrictions on effective population size in the host environment. As a free-living bacterium, Prochlorococcus MED4 is not known to be subject to similar ecological constraints. To test whether the high-light-adapted Prochlorococcus MED4 is experiencing a reduction in selection efficiency resulting from genetic drift, we examine two data sets, namely, the environmental genome shotgun sequencing data from the Sargasso Sea and a set of cyanobacterial genome sequences. After integrating these data sets, we compare the evolutionary profile of a high-light Prochlorococcus group to that of a group of Synechococcus (a closely related group of marine cyanobacteria) that does not exhibit a similar small-genome syndrome. The average pairwise dN/dS ratios in the high-light-adapted Prochlorococcus group are significantly lower than those in the Synechococcus group, leading us to reject the hypothesis that the Prochlorococcus group is currently experiencing higher levels of genetic drift.