Origin and evolution of the ribosome

Abstract

The modern ribosome was largely formed at the time of the last common ancestor, LUCA. Hence its earliest origins likely lie in the RNA world. Central to its development were RNAs that spawned the modern tRNAs and a symmetrical region deep within the large ribosomal RNA, (rRNA), where the peptidyl transferase reaction occurs. To understand pre-LUCA developments, it is argued that events that are coupled in time are especially useful if one can infer a likely order in which they occurred. Using such timing events, the relative age of various proteins and individual regions within the large rRNA are inferred. An examination of the properties of modern ribosomes strongly suggests that the initial peptides made by the primitive ribosomes were likely enriched for l-amino acids, but did not completely exclude d-amino acids. This has implications for the nature of peptides made by the first ribosomes. From the perspective of ribosome origins, the immediate question regarding coding is when did it arise rather than how did the assignments evolve. The modern ribosome is very dynamic with tRNAs moving in and out and the mRNA moving relative to the ribosome. These movements may have become possible as a result of the addition of a template to hold the tRNAs. That template would subsequently become the mRNA, thereby allowing the evolution of the code and making an RNA genome useful. Finally, a highly speculative timeline of major events in ribosome history is presented and possible future directions discussed.

Figure 1.

Assembly map of 50S ribosomal subunit with all nonuniversal protein omitted. The map was derived from Nierhaus (2001) and is a slightly modified version of that presented previously Fox and Naik (2004). Each protein is indicated by a numbered box with the 23S rRNA indicated at the top. Lines with arrows indicate order in assembly with darker lines representing stronger dependencies. Thus L4 and L24 bind directly to the RNA and work together to facilitate the incorporation of L22. Boxes are colored with regard to the similarity of their position in assembly. For example, yellow indicates terminal proteins, which are not required for addition of any other universal protein.

Figure 2.

The secondary structure of Haloarcula marismortui 23S rRNA is broken into six major domains (I through VI) with subregions in the various domains denoted as 1.1, 1.2, etc. The highlighted regions are the most interconnected as measured by the numbers of base-base interactions between a residue in one domain and a residue in another. The figure is taken from Hury et al. 2006.