A neutral process of genome reduction in marine bacterioplankton

Abstract

Marine bacterioplankton communities are dominated by cells equipped with small genomes. Streamlining selection has been accepted as the main force driving their genome reduction. Here, we report that a neutral evolutionary mechanism governs genome reduction in the Roseobacter group that represents 5-20% of the bacterioplankton cells in coastal waters. Using representative strains that fall into three genome size groups (2-3, 3-4, and 4-5 Mbp), we measured their genomic mutation rates (μ) through long-term mutation accumulation experiments followed by genome sequencing the resulting 437 mutant lines. We further calculated their effective population sizes (Ne) based on μ and the neutral genetic diversity of the studied species, the latter estimated based on multiple genome sequences of natural isolates collected from global oceans with their population structure considered. A surprising finding is that Ne scales positively with genome size, which is the opposite of the expectation from the streamlining selection theory. As the strength of random genetic drift is the inverse of Ne, this result instead suggests drift as the primary driver of genome reduction. Additionally, we report a negative scaling between μ and genome size, which is the first experimental evidence for the long-lasting hypothesis that mutation rate increases play a part in marine bacterial genome reduction. As μ scales inversely with Ne, genetic drift appears to be the ultimate cause of genome reduction in these Roseobacters. Our finding discounts, but is insufficient to reject, the streamlining theory because streamlining process is expected to be more effective in oligotrophic open ocean waters.