Identification of a circular code periodicity in the bacterial ribosome: origin of codon periodicity in genes?

Fiche publication

Date publication

janvier 2020

Journal

RNA biology

Auteurs

Membres identifiés du Cancéropôle Est :
Dr THOMPSON Julie

Tous les auteurs :
Michel CJ, Thompson JD

Lien Pubmed

https://www.ncbi.nlm.nih.gov/pubmed/31960748

Résumé

Three-base periodicity (TBP), where nucleotides and higher order -tuples are preferentially spaced by 3, 6, 9, etc. bases, is a well-known intrinsic property of protein-coding DNA sequences. However, its origins are still not fully understood. One hypothesis is that the periodicity reflects a primordial coding system that was used before the emergence of the modern standard genetic code (SGC). Recent evidence suggests that the circular code, a set of 20 trinucleotides allowing the reading frames in genes to be retrieved locally, represents a possible ancestor of the SGC. Motifs from the circular code have been found in the reading frame of protein-coding regions in extant organisms from bacteria to eukaryotes, in many transfer RNA (tRNA) genes and in important functional regions of the ribosomal RNA (rRNA), notably in the peptidyl transferase center and the decoding center (Dila et al., 2019b). Here, we have used a powerful correlation function to search for periodicity patterns involving the 20 trinucleotides of the circular code in a large set of bacterial protein-coding genes, as well as in the translation machinery, including rRNA and tRNA sequences. As might be expected, we found a strong circular code periodicity 0 modulo 3 in the protein-coding genes. More surprisingly, we also identified a similar circular code periodicity in a large region of the 16S rRNA. This region includes the 3' major domain corresponding to the primordial proto-ribosome decoding center and containing numerous sites that interact with the tRNA and messenger RNA (mRNA) during translation. Furthermore, 3D structural analysis shows that the periodicity region surrounds the mRNA channel that lies between the head and the body of the SSU. Our results support the hypothesis that the circular code may constitute an ancestral translation code involved in reading frame retrieval and maintenance, traces of which persist in modern mRNA, tRNA and rRNA despite their long evolution and adaptation to the SGC.