Integrated evolution of ribosomal RNAs, introns, and intron nurseries

Abstract

The initial components of ribosomes first appeared more than 3.8 billion years ago during a time when many types of RNAs were evolving. While modern ribosomes are complex molecular machines consisting of rRNAs and proteins, they were assembled during early evolution by the association and joining of small functional RNA units. Introns may have provided the means to ligate many of these pieces together. All four classes of introns (group I, group II, spliceosomal, and archaeal) are present in many rRNA gene loci over a broad phylogenetic range. A survey of rRNA intron sequences across the three major life domains suggests that some of the classes of introns may have diverged from one another within rRNA gene loci. Analyses of rRNA sequences revealed self-splicing group I and group II introns are present in ancestral regions of the SSU (small subunit) and LSU (large subunit), whereas spliceosomal and archaeal introns appeared in sections of the rRNA that evolved later. Most classes of introns increased in number for approximately 1 billion years. However, their frequencies are low in the most recently evolved regions added to the SSU and LSU rRNAs. Furthermore, many of the introns appear to have been in the same locations for billions of years, suggesting an ancient origin for these sequences. In this Perspectives paper, I reviewed and analyzed rRNA intron sequences, locations, structural characteristics, and splicing mechanisms; and suggest that rRNA gene loci may have served as evolutionary nurseries for intron formation and diversification.

Analysis of Acanthamoeba genotypes from public freshwater sources in Thailand reveals a new genotype, T23 Acanthamoeba bangkokensis sp. nov.

“…Meanwhile, the origin of introns has been suggested to be ancient and could have co-evolved with rRNAs. The presence of introns in the same locations of the rRNA genes across domains of life could imply that their existence predated evolutionary divergence and speciation 33 . It has been suggested that the wide spread occurrence of the S516 intron in various eukaryotes could have arisen from vertical transfer while subsequent loss of the intron could occur later in the evolution 29 , 33 .…”

“…The presence of introns in the same locations of the rRNA genes across domains of life could imply that their existence predated evolutionary divergence and speciation 33 . It has been suggested that the wide spread occurrence of the S516 intron in various eukaryotes could have arisen from vertical transfer while subsequent loss of the intron could occur later in the evolution 29 , 33 . Although intron gain and loss could occur in rRNAs, the lack of intron in all isolates bearing genotypes T4 and T5 in this study could suggest that the former process may not be common among Acanthamoeba bearing these genotypes in Thailand.…”

Mitochondrial genetics revisited

“…These remarkable introns, identified long ago (Michel & Dujon, ), are most frequently encoded by organellar genomes (where they were discovered) but can also be found in bacterial, archaeal, or viral genomes (Hausner, Hafez, & Edgell, ; Nawrocki, Jones, & Eddy, ) as well as in the rDNA of eukaryotic chromosomes (Johansen, Haugen, & Nielsen, ) where they might have originated (Rogers, ). Groups I and II introns form two distinct families of RNA enzymes by their 3D structures and the transesterification reactions catalysed (Adams, Stahley, Kosek, Wang, & Strobel, ; Cech, ; Pyle, ; Robart, Chan, Peters, Rajashankar, & Toor, ).…”

Expansion segments in bacterial and archaeal 5S ribosomal RNAs

“…Even if the extended 5S rRNA genes are properly expressed, the insertions might not be retained in the primary transcripts in the form of expansion segments but excised as it happens with rRNA introns and intervening sequences (Rogers 2019, Evguenieva-Hackenberg 2005. The most solidly confirmed expansion segment is by far the one found in H. morrhuae 5S rRNA.…”