Expansion segments in bacterial and archaeal 5S ribosomal RNAs

Abstract

The large ribosomal RNAs of eukaryotes frequently contain expansion sequences that add to the size of the rRNAs but do not affect their overall structural layout and are compatible with major ribosomal function as an mRNA translation machine. The expansion of prokaryotic ribosomal RNAs is much less explored. In order to obtain more insight into the structural variability of these conserved molecules, we herein report the results of a comprehensive search for the expansion sequences in prokaryotic 5S rRNAs. Overall, 89 expanded 5S rRNAs of 15 structural types were identified in 15 archaeal and 36 bacterial genomes. Expansion segments ranging in length from 13 to 109 residues were found to be distributed among 17 insertion sites. The strains harboring the expanded 5S rRNAs belong to the bacterial orders Clostridiales, Halanaerobiales, Thermoanaerobacterales, and Alteromonadales as well as the archael order Halobacterales. When several copies of a 5S rRNA gene are present in a genome, the expanded versions may coexist with normal 5S rRNA genes. The insertion sequences are typically capable of forming extended helices, which do not seemingly interfere with folding of the conserved core. The expanded 5S rRNAs have largely been overlooked in 5S rRNA databases.

Ribosome Biogenesis in Archaea

“…are characterized by the presence of so-called expansion segments (ES), which are additional RNA elements of various sizes incorporated into the universal prokaryotic rRNA core (Gerbi, 1996;Bowman et al, 2020; Figure 1). These ES increase the size and complexity of the respective rRNAs; however, recent analyses have provided evidence for the presence of such ES in both bacteria and archaea (Armache et al, 2013;Penev et al, 2020;Tirumalai et al, 2020;Stepanov and Fox, 2021). Although most of these sequence additions are limited in size and number (Armache et al, 2013;Penev et al, 2020;Tirumalai et al, 2020;Stepanov and Fox, 2021), larger ES, similar in size to those commonly observed in eukaryotes, have been recently described in the Asgard archaeal phylum (Penev et al, 2020), which is proposed to be the cradle of the eukaryotic lineage (Spang et al, 2015;Zaremba-Niedzwiedzka et al, 2017;.…”

“…These ES increase the size and complexity of the respective rRNAs; however, recent analyses have provided evidence for the presence of such ES in both bacteria and archaea (Armache et al, 2013;Penev et al, 2020;Tirumalai et al, 2020;Stepanov and Fox, 2021). Although most of these sequence additions are limited in size and number (Armache et al, 2013;Penev et al, 2020;Tirumalai et al, 2020;Stepanov and Fox, 2021), larger ES, similar in size to those commonly observed in eukaryotes, have been recently described in the Asgard archaeal phylum (Penev et al, 2020), which is proposed to be the cradle of the eukaryotic lineage (Spang et al, 2015;Zaremba-Niedzwiedzka et al, 2017;. However, a common evolutionary relationshipbased on sequence and/or structure homology-of the larger archaeal and eukaryotic ES could not be established (Penev et al, 2020).…”

Menzerath–Altmann’s Law of Syntax in RNA Accretion History

“…At the molecular evolution level and in the course of typically millions to billions of years, component parts are added to growing molecules, which also interact with other molecules to form complexes and higher-order molecular and cellular structure [2]. In RNA, the mere existence of rare expansion segments protruding in the molecules of selected lineages (e.g., bacterial and archaeal 5S rRNA [3]) suggests tendencies of molecular growth. However, accretion must be made explicit with phylogenetic methods.…”

Features of smaller ribosomes in Candidate Phyla Radiation (CPR) bacteria revealed with a molecular evolutionary analysis

“…Although helix 44 contributes to the accuracy of translation initiation (Qin et al 2012), the position of 16Gap5 does not affect known functional sites. 5Gap1 in the 5S rRNA corresponds to helix IV and loop D, a region that shows large structural variation in bacteria, and can be lost (Szymanski et al 2016; Stepanov and Fox 2021). Some rRNA helices are known to be deleted in small non-CPR genomes (Nikolaeva et al 2021), but no case of 23SGap3 (the loss of 23S rRNA helix 78) has yet been reported.…”