Investment in rapid growth shapes the evolutionary rates of essential proteins

Proteins evolve at very different rates and, most notably, at rates inversely proportional to the level at which they are produced. The relative frequency of highly expressed proteins in the proteome, and thus their impact on the cell budget, increases steeply with growth rate. The maximal growth rate is a key life-history trait reflecting trade-offs between rapid growth and other fitness components. We show that the maximal growth rate is weakly affected by genetic drift. The negative correlation between protein expression levels and evolutionary rate and the positive correlation between expression levels of highly expressed proteins and growth rates, suggest that investment in growth affects the evolutionary rate of proteins, especially the highly expressed ones. Accordingly, analysis of 61 families of orthologs in 74 proteobacteria shows that differences in evolutionary rates between lowly and highly expressed proteins depend on maximal growth rates. Analyses of complexes with key roles in bacterial growth and strikingly different expression levels, the ribosome and the replisome, confirm these patterns and suggest that the growth-related sequence conservation is associated with protein synthesis. Maximal growth rates also shape protein evolution in the other bacterial clades. Long-branch attractions associated with this effect might explain why clades with persistent history of slow growth are attracted to the root when the tree of prokaryotes is inferred using highly, but not lowly, expressed proteins. These results indicate that reconstruction of deep phylogenies can be strongly affected by maximal growth rates, and highlight the importance of life-history traits and their physiological consequences for protein evolution.