Heterogeneity of the translational machinery: Variations on a common theme

Abstract

In all organisms the universal process of protein synthesis is performed by the ribosome, a complex multi-component assembly composed of RNA and protein elements. Although ribosome heterogeneity was observed already more than 40 years ago, the ribosome is still traditionally viewed as an unchangeable entity that has to be equipped with all ribosomal components and translation factors in order to precisely accomplish all steps in protein synthesis. In the recent years this concept was challenged by several studies highlighting a broad variation in the composition of the translational machinery in response to environmental signals, which leads to its adaptation and functional specialization. Here, we summarize recent reports on the variability of the protein synthesis apparatus in diverse organisms and discuss the multiple mechanisms and possibilities that can lead to functional ribosome heterogeneity. Collectively, these results indicate that all cells are equipped with a remarkable toolbox to fine tune gene expression at the level of translation and emphasize the physiological importance of ribosome heterogeneity for the immediate implementation of environmental information.

Keywords: Gene expression regulation; Protein synthesis; Ribosome heterogeneity; Stress response; Translation regulation.

Fig. 1

Scientific publications addressing ‘ribosome heterogeneity’ since 1969. The graph depicts that despite being already observed more than 40 years ago, ribosome heterogeneity as a means to regulate translation was not a scientific subject till the dawn of the new millennium.

Fig. 2

Components of the translation machinery that have the potential to contribute to functional heterogeneity. Structures were visualized with Polyview 3D software [125] using the following maps: E. coli large ribosomal subunit (LSU; pdb accession code: 3d5a [126], rRNA in light gray, proteins in dark gray); small ribosomal subunit (SSU; pdb accession code: 3d5b [126]); E. coli IF2 (pdb accession code: 1g7r [127]); human eIF3 (EMD-2166 [128]); yeast tRNA^Phe (pdb accession code: 6tna [129]).