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Noncanonical features and modifications on the 5′‐end of bacterial sRNAs and mRNAs

Advanced Review

Alexander Serganov, Ang Gao, Nikita Vasilyev

Published Online: Oct 01 2018

DOI: 10.1002/wrna.1509

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Although many eukaryotic transcripts contain cap structures, it has been long thought that bacterial RNAs do not carry any special modifications on their 5′‐ends. In bacteria, primary transcripts are produced by transcription initiated with a nucleoside triphosphate and are therefore triphosphorylated on 5′‐ends. Some transcripts are then processed by nucleases that yield monophosphorylated RNAs for specific cellular activities. Many primary transcripts are also converted to monophosphorylated species by removal of the terminal pyrophosphate for 5′‐end‐dependent degradation. Recent studies surprisingly revealed an expanded repertoire of chemical groups on 5′‐ends of bacterial RNAs. In addition to mono‐ and triphosphorylated moieties, some mRNAs and sRNAs contain cap‐like structures and diphosphates on their 5′‐ends. Although incorporation and removal of these groups have become better understood in recent years, the physiological significance of these modifications remain obscure. This review highlights recent studies aimed at identification and elucidation of novel modifications on the 5′‐ends of bacterial RNAs and discusses possible physiological applications of the modified RNAs. This article is categorized under: RNA Turnover and Surveillance > Regulation of RNA Stability RNA Structure and Dynamics > RNA Structure, Dynamics, and Chemistry RNA Processing > Capping and 5′ End Modifications

Typical 5′‐ends of mRNA. (a) A cap structure on mRNA of eukaryotes and (b) a triphosphorylated end of primary bacterial transcripts

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Structures of the E. coli NudC enzyme. (a) Overall structure of the NudC dimer (Hofer et al., ). Bound NAD is shown in stick representation and atomic colors (carbon, yellow; oxygen, red; nitrogen, blue; phosphorus, orange). (b) Zoomed‐in view of the NAD‐binding site. NADs from two available structures are superposed and shown in different colors of carbon atoms (yellow, ref. Zhang et al., ; magenta, ref. Hofer et al., ). Intermolecular hydrogen bonds are depicted by black dashed lines. Amino acids shown in sticks are glutamates involved in catalysis and aromatic residues involved in stacking with the adenine base of NAD. (c) Superposition of NudC (green) (Zhang et al., ) and RppH (brown) (Vasilyev & Serganov, ) on the Nudix helix. RppH‐bound RNA is in blue, and Mg²⁺ cations from the RppH structure are in magenta. (d) Superposition of the reaction substrate NAD (yellow) (Zhang et al., ) and reaction product NMN (cyan) (Hofer et al., ) in the NudC structures. (e) Electrostatic surface view of the catalytic pocket of NudC bound to NAD (yellow) (Zhang et al., ). The view shows that the pocket can accommodate dpCoA (violet), which was modeled based on the NudC‐NAD structure (Zhang et al., )

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Structural basis of NCIN‐mediated transcription initiation. (a) Crystal structures of Tth RNAP bound to pppApC (Bird et al., ). DNA is in gray. RNA is shown in atomic colors: Cyan, carbon; orange, phosphorus; red, oxygen; blue, nitrogen atoms. Protein is in atomic colors with carbon atoms in green. Hydrogen bonds are shown by dark blue dashed lines. The Mg²⁺ cation is depicted as a green sphere. NA, nicotinamide. (b) Crystal structures of Tth RNAP bound to NAD + pC (Bird et al., ). A red sphere represents a water molecule

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Noncanonical caps on bacterial mRNAs. (a) Cap structures identified experimentally in E. coli (Chen et al., ; Kowtoniuk et al., ). (b) Nucleotide derivatives which Eco RNAP can use for transcription in vitro (Julius & Yuzenkova, )

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Structures of E. coli RppH. (a) Structure of pppAGU‐bound RppH (cyan sticks) shown with electrostatic surface representation of the protein (Vasilyev & Serganov, ). Mg²⁺ cations are depicted as magenta spheres. (b) A view of the RNA‐binding cleft. Amino acids recognizing guanosine and adjacent moieties are in sticks. Intermolecular hydrogen bond and cation‐π interactions are shown as black and red dashed lines, respectively. (c) Active site of RppH. Hydrogen bonds between RNA and RppH are shown as black dashed lines. Coordination bonds between RNA and Mg²⁺ cations are shown as red dashed lines. A water molecule likely involved in catalysis is shown as a red sphere. A black arrow shows in‐line attack of the water molecule on the β phosphorus atom. (d) Structure of the ternary E. coli RppH‐RNA‐DapF complex with RNA (red sticks) bound to RppH (Gao et al., )

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RNA degradation pathways in E. coli. (a) Direct access pathway. The pathway begins with the initial internal cleavage by RNase E. The resulting 5′‐fragment is then degraded by 3′‐end‐dependent exonucleases while the 3′‐fragment, typically protected from exonucleases by a stem‐loop structure on the 3′‐end, is subjected to new rounds of RNase E/exonuclease cleavage. (b) 5′‐End‐dependent pathway. In E. coli, this pathway begins with conversion of 5′‐triphosphorylated RNAs to monophosphorylated species, a process that involves the activity of RppH. The monophosphorylated RNAs are optimal substrates for 5′‐end‐dependent RNase E cleavage, followed by rounds of RNaseE/exonuclease digestion. (c) Recent modifications of the 5′‐end‐dependent RNA degradation pathway of E. coli. Conversion of the triphosphorylated 5′‐ends of primary transcripts to monophosphorylated species requires the consecutive removal of phosphate by an unknown enzyme(s) and RppH. DapF stimulates RppH activity

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