On the Origin of Compositional Features of Ribosomes

Ribosomes are highly abundant in cells and comprise, besides RNAs of varying lengths, 55-80 similarly sized, short proteins. This seemingly unusual composition is thought to have resulted from selection for rapid autocatalytic ribosome production. Here, we demonstrate that ribosomal protein-splitting mutations cannot accelerate ribosome production. The autocatalytic explanation is also unnecessary, because protein lengths generally decline with expression levels. Although ribosomal proteins are shorter than expected from their expression levels, they are not outliers among members of large protein complexes in mean protein length or coefficient of variation. These observations are explainable because 1) shortening proteins lowers their synthetic cost and reduces the waste from mistranslation-induced protein dysfunction and degradation, 2) such benefits rise with expression levels, and 3) members of large complexes participate in more protein-protein interactions so are less tolerant to mistranslation. These and other considerations suggest that the compositional features of ribosomes originate from cellular energy economics.