Chapter 21 : Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics

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In contrast to most bacterial noncoding RNAs (ncRNAs) ( ), Y RNAs were initially characterized in human cells and only later shown to exist in bacteria. The human RNAs were discovered because they are found complexed with the Ro 60-kDa autoantigen (Ro60), a ring-shaped protein that is a clinically important target of autoantibodies in patients with two systemic autoimmune rheumatic diseases, systemic lupus erythematosus and Sjögren’s syndrome ( ). Y RNAs and their Ro60 protein partner were subsequently shown to be present in all examined animal cells as well as in a subset of bacteria ( ). The number of distinct Y RNAs varies between species, with most characterized organisms having between two and four ( ). Although all experimentally verified Y RNAs are between 69 and 150 nucleotides, homology searches predict that some bacterial Y RNAs may exceed 200 nucleotides ( ).

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
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Figure 1

Predicted secondary structures of a human Y RNA and the experimentally identified bacterial Y RNAs. (A) Human Y3 RNA. Modules involved in binding Ro60 and effector proteins are indicated. The portion of the stem containing the Ro60 binding site can form an alternative conformer containing a conserved bulged helix ( ). In the structure of Y3 complexed with Ro60 ( ), the bases shown in green (GGUCCGA) are sites of specific interactions with the Ro60 protein. (B, C) Yrn1 and Yrn2. The sequences that can form the conserved helix are boxed, and the conserved “metazoan motif” GGUCCGA is colored in green. An adenine nucleotide that may represent the second A in the “bacterial motif” is colored orange. On Yrn1, regions for Rsr binding and PNPase binding are indicated. (D, E) Typhimurium YrlA and YrlB. The GNCGAANG motif is in orange. (F, G) YrlA and YrlB. Nucleotides are colored as in panels D and E.

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
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Figure 2

Structures of Ro60 and Rsr proteins. (A) A molecular surface representation of Ro60 (PDB ID: 1YVR) colored by electrostatic surface potential. (B) A molecular surface representation of Rsr (PDB ID: 2NVO) colored by electrostatic surface potential. For both panels A and B, positive potentials are in blue and negative potentials are in red (–10 kT/e to 10 kT/e). (C) Structure of Ro60 bound to a misfolded 5S rRNA fragment (PDB ID: 2I91). The helix binds the basic outer surface and the single-stranded 3′ end binds in the hole. (D) Structure of Ro60 bound to a fragment of Y RNA stem containing the conserved sequences required for Ro60 binding (PDB ID: 1YVP). Positions of the 5′ and 3′ ends are indicated. Biochemical studies support a model in which other portions of the Y RNA contact a basic platform that overlaps with the misfolded RNA-binding site (dashed line) ( ).

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
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Figure 3

YrlA RNAs contain a module that resembles tRNA. (A) Typhimurium YrlA presented to resemble a canonical tRNA. Highly conserved nucleotides between YrlA orthologs are colored orange, while conserved purines and pyrimidines are in blue. Bases shown to be modified ( ) are indicated. AS, D, T, and V denote the acceptor stem, D arm, T arm, and variable arm, respectively. (B) tRNA-Ala-GCA. Nucleotides that are conserved between YrlA RNAs are in orange. All depicted tertiary interactions can potentially form in YrlA RNAs. (C) The genome-encoded sequence of YrlA drawn to emphasize the resemblance to tRNA. The structure of the acceptor stem after cleavage, end nibbling, and posttranscriptional CA addition ( ) is also shown (arrow). Conserved nucleotides are colored as in panel A. (D) Yrn1 presented to resemble tRNA. Nucleotides in the T arm that are conserved between Yrn1 and YrlA RNAs are colored as in panel A.

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
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Figure 4

Phylogenetic trees of representative Rsr-containing bacterial species. (A) Phylogenetic tree based on the sequences of 16S rRNAs ( ). Each phylum is represented by a distinct color. (B) Phylogenetic tree based on the sequences of Rsr proteins. Sequence alignments were performed using Clustal Omega ( ), and trees were drawn with the Phylogeny Interference Package (PHYLIP) using the maximum likelihood method ( ).

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
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Figure 5

Role of Yrn1 in scaffolding RYPER formation. (A) Yrn1, Rsr (PDB ID: 2NVO) (light blue), and PNPase (PDB ID: 1E3P) (pink). The Yrn1 modules that bind Rsr and PNPase are indicated. (B) The structure of RYPER predicted by single-particle electron microscopy and three-dimensional reconstruction ( ) (EMDB ID: 5389). The density that likely corresponds to Yrn1 is colored in yellow, while densities corresponding to Rsr and PNPase are colored as in panel A. A possible path for degrading a structured RNA substrate, in which the 3′ end threads from Rsr into the PNPase cavity for degradation, is depicted in blue.

Citation: Sim S, Wolin S. 2019. Bacterial Y RNAs: Gates, Tethers, and tRNA Mimics, p 369-381. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0023-2018
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