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C/D box sRNA-guided 2'-O-methylation patterns of archaeal rRNA molecules.

Dennis PP, Tripp V, Lui L, Lowe T, Randau L - BMC Genomics (2015)

Bottom Line: We propose that they act as RNA chaperones and facilitate complex folding events between distant sequences.This 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.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse 10, 35043, Marburg, Germany. dennisp@janelia.hhmi.org.

ABSTRACT

Background: 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. 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.

Results: We 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.

Conclusions: This 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.

No MeSH data available.


Related in: MedlinePlus

Distribution of 2′-O-ribose methylation sites in archaeal 16S rRNA. Predicted sites of sRNA directed 2′-O-ribose methylation (Additional Files 1 and 4) from seven archaeal species listed in Table 1 were mapped onto the consensus secondary structure of the archaeal 16S rRNA [21]. The multiple occurrences of methylation at a given nucleotide position is indicated by increasing dot size (i.e. methylation targets found in one to six organisms). The color of the dots (from blue to red) indicates increasing methylation frequency within a nine nucleotide window. The archaeal nucleotide alignment positions of sites of modification discussed in the context of 16S rRNA structure-function are indicated
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Fig2: Distribution of 2′-O-ribose methylation sites in archaeal 16S rRNA. Predicted sites of sRNA directed 2′-O-ribose methylation (Additional Files 1 and 4) from seven archaeal species listed in Table 1 were mapped onto the consensus secondary structure of the archaeal 16S rRNA [21]. The multiple occurrences of methylation at a given nucleotide position is indicated by increasing dot size (i.e. methylation targets found in one to six organisms). The color of the dots (from blue to red) indicates increasing methylation frequency within a nine nucleotide window. The archaeal nucleotide alignment positions of sites of modification discussed in the context of 16S rRNA structure-function are indicated

Mentions: To identify the distribution and conservation of sites of rRNA methylation, we first generated alignments of the respective 16S and 23S rRNA sequences from the seven divergent species of archaea (Additional files 3 and 4). The 719 predicted positions of modification (listed in Additional file 1) from the seven species were mapped onto the universal alignment and then located on secondary structure maps of 16S and 23S rRNA (Figs. 1 and 2). There were 266 predicted modifications in 16S rRNA that occur at 195 different positions and 453 predicted modifications in 23S rRNA that occur at 334 different positions. In 16S and 23S rRNA there are respectively 152 and 255 sites that are unique and modified in only a single species. In addition, there are 43 and 79 sites in the respective 16S and 23S rRNA sequences that are modified in two or more of the species.Fig. 1


C/D box sRNA-guided 2'-O-methylation patterns of archaeal rRNA molecules.

Dennis PP, Tripp V, Lui L, Lowe T, Randau L - BMC Genomics (2015)

Distribution of 2′-O-ribose methylation sites in archaeal 16S rRNA. Predicted sites of sRNA directed 2′-O-ribose methylation (Additional Files 1 and 4) from seven archaeal species listed in Table 1 were mapped onto the consensus secondary structure of the archaeal 16S rRNA [21]. The multiple occurrences of methylation at a given nucleotide position is indicated by increasing dot size (i.e. methylation targets found in one to six organisms). The color of the dots (from blue to red) indicates increasing methylation frequency within a nine nucleotide window. The archaeal nucleotide alignment positions of sites of modification discussed in the context of 16S rRNA structure-function are indicated
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4644070&req=5

Fig2: Distribution of 2′-O-ribose methylation sites in archaeal 16S rRNA. Predicted sites of sRNA directed 2′-O-ribose methylation (Additional Files 1 and 4) from seven archaeal species listed in Table 1 were mapped onto the consensus secondary structure of the archaeal 16S rRNA [21]. The multiple occurrences of methylation at a given nucleotide position is indicated by increasing dot size (i.e. methylation targets found in one to six organisms). The color of the dots (from blue to red) indicates increasing methylation frequency within a nine nucleotide window. The archaeal nucleotide alignment positions of sites of modification discussed in the context of 16S rRNA structure-function are indicated
Mentions: To identify the distribution and conservation of sites of rRNA methylation, we first generated alignments of the respective 16S and 23S rRNA sequences from the seven divergent species of archaea (Additional files 3 and 4). The 719 predicted positions of modification (listed in Additional file 1) from the seven species were mapped onto the universal alignment and then located on secondary structure maps of 16S and 23S rRNA (Figs. 1 and 2). There were 266 predicted modifications in 16S rRNA that occur at 195 different positions and 453 predicted modifications in 23S rRNA that occur at 334 different positions. In 16S and 23S rRNA there are respectively 152 and 255 sites that are unique and modified in only a single species. In addition, there are 43 and 79 sites in the respective 16S and 23S rRNA sequences that are modified in two or more of the species.Fig. 1

Bottom Line: We propose that they act as RNA chaperones and facilitate complex folding events between distant sequences.This 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.

View Article: PubMed Central - PubMed

Affiliation: Max-Planck-Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse 10, 35043, Marburg, Germany. dennisp@janelia.hhmi.org.

ABSTRACT

Background: 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. 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.

Results: We 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.

Conclusions: This 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.

No MeSH data available.


Related in: MedlinePlus