Abstract

BackgroundIn archaea and eukaryotes, ribonucleoprotein complexes containing small C/D box s(no)RNAs use base pair complementarity to target specific sites within ribosomal RNA for 2'-O-ribose methylation. These modifications aid in the folding and stabilization of nascent rRNA molecules and their assembly into ribosomal particles. The genomes of hyperthermophilic archaea encode large numbers of C/D box sRNA genes, suggesting an increased necessity for rRNA stabilization at extreme growth temperatures.ResultsWe have identified the complete sets of C/D box sRNAs from seven archaea using RNA-Seq methodology. In total, 489 C/D box sRNAs were identified, each containing two guide regions. A combination of computational and manual analyses predicts 719 guide interactions with 16S and 23S rRNA molecules. This first pan-archaeal description of guide sequences identifies (i) modified rRNA nucleotides that are frequently conserved between species and (ii) regions within rRNA that are hotspots for 2'-O-methylation. Gene duplication, rearrangement, mutational drift and convergent evolution of sRNA genes and guide sequences were observed. In addition, several C/D box sRNAs were identified that use their two guides to target locations distant in the rRNA sequence but close in the secondary and tertiary structure. We propose that they act as RNA chaperones and facilitate complex folding events between distant sequences.ConclusionsThis pan-archaeal analysis of C/D box sRNA guide regions identified conserved patterns of rRNA 2'-O-methylation in archaea. The interaction between the sRNP complexes and the nascent rRNA facilitates proper folding and the methyl modifications stabilize higher order rRNA structure within the assembled ribosome.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1839-z) contains supplementary material, which is available to authorized users.

Highlights

  • In archaea and eukaryotes, ribonucleoprotein complexes containing small C/D box s(no)RNAs use base pair complementarity to target specific sites within ribosomal RNA for 2'-O-ribose methylation

  • Included is Nanoarchaeum equitans, a hyperthermophilic archaeon with a highly compacted genome of only 490 kb size which harbors a small set of only 26 C/D box Small RNA (sRNA) genes under genome reduction constraints

  • These observations are in agreement with an increased need for 2'-O-methylated nucleotides in ribosomal RNA (rRNA) regions that lack protein protection to stabilize these sequences at high temperatures

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Summary

Introduction

Ribonucleoprotein complexes containing small C/D box s(no)RNAs use base pair complementarity to target specific sites within ribosomal RNA for 2'-O-ribose methylation. These modifications aid in the folding and stabilization of nascent rRNA molecules and their assembly into ribosomal particles. Stable RNA molecules frequently undergo post-transcriptional modifications The majority of these modifications involve the addition of methyl groups. Eukaryotes and archaea utilize ribonucleoprotein (RNP) complexes containing small (s)RNAs to identify targets for 2'-O-methylation. These sRNA molecules are called small nucleolar RNAs (C/D box snoRNA) in eukaryotes

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