The role of mRNA structure in bacterial translational regulation

Advanced Review

Michelle M. Meyer

Published Online: Jun 14 2016

DOI: 10.1002/wrna.1370

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The characteristics of bacterial messenger RNAs (mRNAs) that influence translation efficiency provide many convenient handles for regulation of gene expression, especially when coupled with the processes of transcription termination and mRNA degradation. An mRNA's structure, especially near the site of initiation, has profound consequences for how readily it is translated. This property allows bacterial gene expression to be altered by changes to mRNA structure induced by temperature, or interactions with a wide variety of cellular components including small molecules, other RNAs (such as sRNAs and tRNAs), and RNA‐binding proteins. This review discusses the links between mRNA structure and translation efficiency, and how mRNA structure is manipulated by conditions and signals within the cell to regulate gene expression. The range of RNA regulators discussed follows a continuum from very complex tertiary structures such as riboswitch aptamers and ribosomal protein‐binding sites to thermosensors and mRNA:sRNA interactions that involve only base‐pairing interactions. Furthermore, the high degrees of diversity observed for both mRNA structures and the mechanisms by which inhibition of translation occur have significant consequences for understanding the evolution of bacterial translational regulation. WIREs RNA 2017, 8:e1370. doi: 10.1002/wrna.1370 This article is categorized under: RNA Structure and Dynamics > Influence of RNA Structure in Biological Systems RNA Evolution and Genomics > RNA and Ribonucleoprotein Evolution Translation > Translation Mechanisms

Mechanisms for translation inhibition by protein binding. (a) The ‘displacement’ or competitive mechanism, exemplified by the L1 (rplK, rplA) regulator in Escherichia coli. The 30S subunit and L1 protein compete for the mRNA. 30S subunit binding results in translation. Transcripts bound by L1 and not translated are degraded. (b) The L1 mRNA‐ and (c) rRNA (23S)‐binding sites show significant similarities (highlighted in red). Regulatory features such as SD sequence and translation initiation site are highlighted. (d) The ‘entrapment’ mechanism exemplified by the S15 (rpsO) regulator in E. coli. The 30S subunit interacts with the mRNA and translation may be mediated by S1 interactions. On S15 interaction with the mRNA, the preinitiation complex is trapped in the ternary complex. (e) The S15 regulatory mRNA and (f) rRNA (16S)‐binding site show limited similarity (highlighted in red). (g) Mechanism of ThrS inhibition of translation. ThrS binding prevents 30S subunit interaction and results in rapid mRNA degradation. (h) ThrS mRNA binding site and (i) its substrate, tRNA^thr with similarities highlighted in red.

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Trans‐acting sRNAs offer nuanced responses. (a) Several different sRNAs interact with the rpoS transcript to activate translation initiation through interactions with an mRNA secondary structure that inhibits translation. Each of these RNAs (RprA, DsrA, and ArcZ) has a distinct secondary structure containing a different sequence (colored portions) that interacts with the rpoS transcript to prevent the formation of an SD‐occluding helix within the rpoS transcript. (b) Spot42 regulates many transcripts using several distinct regions within its sequence. These regions are highlighted by the colored nucleotides on the Spot42 structure (left) and a few of the diverse targets of these regions are illustrated (right).

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RNA regulators exhibit a range of complexity. For each RNA regulator, a three‐dimensional structure and its corresponding secondary structure are shown. Bases directly interacting with a ligand are colored red, ligands are colored in blue or green, nucleotides that are not within the crystal structure are in gray (alternative sequences used for crystallization are indicated in boxes), and regulatory features (SD sequence or initiation codon) are shown where appropriate. (a) Mini‐ROSE thermosensor. (b) Solution structure of the mini‐ROSE thermosensor (pdb: 2gio). (c) hncA mRNA containing two CsrA‐binding sites. Second site not in structure pictured is highlighted by red box. (d) Solution structure of CsrA homolog RsmA from Pseudomonas fluorescences with two identical hncA RNA sequences (pdb: 2jpp). (e) L1 mRNA‐binding site from Methanococcus vannielii. (f) The crystal structure of Thermus thermophilus L1 in complex with this mRNA (pdb: 2hw8; see Figure for L1‐binding site from E. coli). (g) SMK‐box, S‐adenosyl methionine riboswitch (SAM) from Enterobacter faecalis. (h) Crystal structure of the SMK‐box interacting with SAM (pdb:3e5c). (i) Cobalamin riboswitch aptamer from Thermoanaerobacter tengcongenesis. (j) Crystal structure of the cobalamin aptamer bound to adenosylcobalamin (pdb: 4gxy).

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