An Important Role for Purifying Selection in Archaeal Genome Evolution

As the null hypothesis of genome evolution, population genetic theory suggests that selection strength controls genome size. Through the process of genetic drift, this theory predicts that compact genomes are maintained by strong purifying selection while complex genomes are enabled by weak purifying selection. It offers a unifying framework that explains why prokaryotic genomes are much smaller than their eukaryotic counterparts. However, recent findings suggest that bigger prokaryotic genomes appear to experience stronger purifying selection, indicating that purifying selection may not dominate prokaryotic genome evolution. Since archaeal genomes were underrepresented in those studies, generalization of the conclusions to both archaeal and bacterial genomes may not be warranted. In this study, we revisited this matter by focusing on archaeal and bacterial genomes separately. We found that bigger bacterial genomes indeed experienced stronger purifying selection, but the opposite was observed in archaeal genomes. This new finding would predict an enrichment of noncoding sequences in large archaeal genomes, which was confirmed by an analysis of coding density. In contrast, coding density remained stable regardless of bacterial genome size. In conclusion, this study suggests that purifying selection may play a more important role in archaeal genome evolution than previously hypothesized, indicating that there could be a major difference between the evolutionary regimes of Archaea and Bacteria. IMPORTANCE The evolution of genome complexity is a fundamental question in biology. A hallmark of eukaryotic genome complexity is that larger genomes tend to have more noncoding sequences, which are believed to be minimal in archaeal and bacterial genomes. However, we found that archaeal genomes also possessed this eukaryotic feature while bacterial genomes did not. This could be predicted from our analysis on genetic drift, which showed a relaxation of purifying selection in larger archaeal genomes, also a eukaryotic feature. In contrast, the opposite was evident in bacterial genomes.