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Secondary structure and domain architecture of the 23S and 5S rRNAs.

Petrov AS, Bernier CR, Hershkovits E, Xue Y, Waterbury CC, Hsiao C, Stepanov VG, Gaucher EA, Grover MA, Harvey SC, Hud NV, Wartell RM, Fox GE, Williams LD - Nucleic Acids Res. (2013)

Bottom Line: We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness.The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed.Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted.

View Article: PubMed Central - PubMed

Affiliation: School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA 30332, USA, Center for Ribosomal Origins and Evolution, Georgia Institute of Technology, Atlanta, GA 30332, USA, School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA, Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA and School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.

ABSTRACT
We present a de novo re-determination of the secondary (2°) structure and domain architecture of the 23S and 5S rRNAs, using 3D structures, determined by X-ray diffraction, as input. In the traditional 2° structure, the center of the 23S rRNA is an extended single strand, which in 3D is seen to be compact and double helical. Accurately assigning nucleotides to helices compels a revision of the 23S rRNA 2° structure. Unlike the traditional 2° structure, the revised 2° structure of the 23S rRNA shows architectural similarity with the 16S rRNA. The revised 2° structure also reveals a clear relationship with the 3D structure and is generalizable to rRNAs of other species from all three domains of life. The 2° structure revision required us to reconsider the domain architecture. We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness. The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed. Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted. Editable 2° structures mapped with various data are provided (http://apollo.chemistry.gatech.edu/RibosomeGallery).

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The 2° structure3D. The revised 2° structure of the 23S and 5S rRNAs of E. coli, is consistent with 3D structures. Domain 0 (orange) forms the central core of the 23S rRNA, to which all other domains are rooted. Domains 0–VI are colored as in Figure 1b. The 5S rRNA is placed in proximity to Helix 39 to reflect their locations in 3D space. The sequences of 23S and 5S rRNAs, the helix numbers and the domains are indicated. To preserve the traditional style of the 23S rRNA layout, Helix 49b is represented by base pairing lines across a loop in Domain III.
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gkt513-F5: The 2° structure3D. The revised 2° structure of the 23S and 5S rRNAs of E. coli, is consistent with 3D structures. Domain 0 (orange) forms the central core of the 23S rRNA, to which all other domains are rooted. Domains 0–VI are colored as in Figure 1b. The 5S rRNA is placed in proximity to Helix 39 to reflect their locations in 3D space. The sequences of 23S and 5S rRNAs, the helix numbers and the domains are indicated. To preserve the traditional style of the 23S rRNA layout, Helix 49b is represented by base pairing lines across a loop in Domain III.

Mentions: A subset of rRNA within the core of the LSU appears to be compact and autonomous and fits criteria for a domain. This subset of the 23S rRNA is called Domain 0. To conceptually create Domain 0 from the domains of the traditional model, we formed Helices 25a and 26a from single strands and appropriated Helix 26 from Domain II, Helix 61 from Domain IV and Helices 72 and 73 from Domain V (Figures 4 and 5, Table 2). The apparently single-stranded extension on Helix 61 (Figure 4a) is tightly coiled onto other elements of the Domain 0 (Figure 4b and c). Similarly, the apparently single-stranded extensions of Helix 26 fold back on each other and on the terminus of Helix 26. The location and interactions of Domain 0 with other domains are illustrated in 3D in the Supplementary Figures S1 and S2. Domain 0 corresponds well with the ancestral core of the LSU in the Bokov and Steinberg model of ribosomal evolution (42).Figure 4.


Secondary structure and domain architecture of the 23S and 5S rRNAs.

Petrov AS, Bernier CR, Hershkovits E, Xue Y, Waterbury CC, Hsiao C, Stepanov VG, Gaucher EA, Grover MA, Harvey SC, Hud NV, Wartell RM, Fox GE, Williams LD - Nucleic Acids Res. (2013)

The 2° structure3D. The revised 2° structure of the 23S and 5S rRNAs of E. coli, is consistent with 3D structures. Domain 0 (orange) forms the central core of the 23S rRNA, to which all other domains are rooted. Domains 0–VI are colored as in Figure 1b. The 5S rRNA is placed in proximity to Helix 39 to reflect their locations in 3D space. The sequences of 23S and 5S rRNAs, the helix numbers and the domains are indicated. To preserve the traditional style of the 23S rRNA layout, Helix 49b is represented by base pairing lines across a loop in Domain III.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3753638&req=5

gkt513-F5: The 2° structure3D. The revised 2° structure of the 23S and 5S rRNAs of E. coli, is consistent with 3D structures. Domain 0 (orange) forms the central core of the 23S rRNA, to which all other domains are rooted. Domains 0–VI are colored as in Figure 1b. The 5S rRNA is placed in proximity to Helix 39 to reflect their locations in 3D space. The sequences of 23S and 5S rRNAs, the helix numbers and the domains are indicated. To preserve the traditional style of the 23S rRNA layout, Helix 49b is represented by base pairing lines across a loop in Domain III.
Mentions: A subset of rRNA within the core of the LSU appears to be compact and autonomous and fits criteria for a domain. This subset of the 23S rRNA is called Domain 0. To conceptually create Domain 0 from the domains of the traditional model, we formed Helices 25a and 26a from single strands and appropriated Helix 26 from Domain II, Helix 61 from Domain IV and Helices 72 and 73 from Domain V (Figures 4 and 5, Table 2). The apparently single-stranded extension on Helix 61 (Figure 4a) is tightly coiled onto other elements of the Domain 0 (Figure 4b and c). Similarly, the apparently single-stranded extensions of Helix 26 fold back on each other and on the terminus of Helix 26. The location and interactions of Domain 0 with other domains are illustrated in 3D in the Supplementary Figures S1 and S2. Domain 0 corresponds well with the ancestral core of the LSU in the Bokov and Steinberg model of ribosomal evolution (42).Figure 4.

Bottom Line: We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness.The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed.Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted.

View Article: PubMed Central - PubMed

Affiliation: School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, GA 30332, USA, Center for Ribosomal Origins and Evolution, Georgia Institute of Technology, Atlanta, GA 30332, USA, School of Chemical and Biomolecular Engineering, Georgia Institute of Technology, Atlanta, GA 30332, USA, Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA and School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.

ABSTRACT
We present a de novo re-determination of the secondary (2°) structure and domain architecture of the 23S and 5S rRNAs, using 3D structures, determined by X-ray diffraction, as input. In the traditional 2° structure, the center of the 23S rRNA is an extended single strand, which in 3D is seen to be compact and double helical. Accurately assigning nucleotides to helices compels a revision of the 23S rRNA 2° structure. Unlike the traditional 2° structure, the revised 2° structure of the 23S rRNA shows architectural similarity with the 16S rRNA. The revised 2° structure also reveals a clear relationship with the 3D structure and is generalizable to rRNAs of other species from all three domains of life. The 2° structure revision required us to reconsider the domain architecture. We partitioned the 23S rRNA into domains through analysis of molecular interactions, calculations of 2D folding propensities and compactness. The best domain model for the 23S rRNA contains seven domains, not six as previously ascribed. Domain 0 forms the core of the 23S rRNA, to which the other six domains are rooted. Editable 2° structures mapped with various data are provided (http://apollo.chemistry.gatech.edu/RibosomeGallery).

Show MeSH