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Enzymes Involved in Posttranscriptional RNA Metabolism in Gram-Negative Bacteria

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  • Authors: Bijoy K. Mohanty1, Sidney R. Kushner2,3
  • Editors: Gisela Storz4, Kai Papenfort5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Genetics; 2: Department of Genetics; 3: Department of Microbiology, University of Georgia, Athens, GA 30602; 4: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 5: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0011-2017
  • Received 16 November 2017 Accepted 24 January 2018 Published 20 April 2018
  • Sidney R. Kushner, [email protected]
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  • Abstract:

    Gene expression in Gram-negative bacteria is regulated at many levels, including transcription initiation, RNA processing, RNA/RNA interactions, mRNA decay, and translational controls involving enzymes that alter translational efficiency. In this review, we discuss the various enzymes that control transcription, translation, and RNA stability through RNA processing and degradation. RNA processing is essential to generate functional RNAs, while degradation helps control the steady-state level of each individual transcript. For example, all the pre-tRNAs are transcribed with extra nucleotides at both their 5′ and 3′ termini, which are subsequently processed to produce mature tRNAs that can be aminoacylated. Similarly, rRNAs that are transcribed as part of a 30S polycistronic transcript are matured to individual 16S, 23S, and 5S rRNAs. Decay of mRNAs plays a key role in gene regulation through controlling the steady-state level of each transcript, which is essential for maintaining appropriate protein levels. In addition, degradation of both translated and nontranslated RNAs recycles nucleotides to facilitate new RNA synthesis. To carry out all these reactions, Gram-negative bacteria employ a large number of endonucleases, exonucleases, RNA helicases, and poly(A) polymerase, as well as proteins that regulate the catalytic activity of particular RNases. Under certain stress conditions, an additional group of specialized endonucleases facilitate the cell’s ability to adapt and survive. Many of the enzymes, such as RNase E, RNase III, polynucleotide phosphorylase, RNase R, and poly(A) polymerase I, participate in multiple RNA processing and decay pathways.

  • Citation: Mohanty B, Kushner S. 2018. Enzymes Involved in Posttranscriptional RNA Metabolism in Gram-Negative Bacteria. Microbiol Spectrum 6(2):RWR-0011-2017. doi:10.1128/microbiolspec.RWR-0011-2017.

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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0011-2017
2018-04-20
2019-10-15

Abstract:

Gene expression in Gram-negative bacteria is regulated at many levels, including transcription initiation, RNA processing, RNA/RNA interactions, mRNA decay, and translational controls involving enzymes that alter translational efficiency. In this review, we discuss the various enzymes that control transcription, translation, and RNA stability through RNA processing and degradation. RNA processing is essential to generate functional RNAs, while degradation helps control the steady-state level of each individual transcript. For example, all the pre-tRNAs are transcribed with extra nucleotides at both their 5′ and 3′ termini, which are subsequently processed to produce mature tRNAs that can be aminoacylated. Similarly, rRNAs that are transcribed as part of a 30S polycistronic transcript are matured to individual 16S, 23S, and 5S rRNAs. Decay of mRNAs plays a key role in gene regulation through controlling the steady-state level of each transcript, which is essential for maintaining appropriate protein levels. In addition, degradation of both translated and nontranslated RNAs recycles nucleotides to facilitate new RNA synthesis. To carry out all these reactions, Gram-negative bacteria employ a large number of endonucleases, exonucleases, RNA helicases, and poly(A) polymerase, as well as proteins that regulate the catalytic activity of particular RNases. Under certain stress conditions, an additional group of specialized endonucleases facilitate the cell’s ability to adapt and survive. Many of the enzymes, such as RNase E, RNase III, polynucleotide phosphorylase, RNase R, and poly(A) polymerase I, participate in multiple RNA processing and decay pathways.

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Figures

Image of FIGURE 1
FIGURE 1

Venn diagram of RNases in showing their involvement in the four major RNA metabolic pathways in Gram-negative bacteria. The participation of the various proteins is only included in pathways where it has been established that they play a significant role. In addition, it is possible that some proteins, such as YbeY, are involved in additional pathways.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0011-2017
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Image of FIGURE 2
FIGURE 2

Model for the initiation of mRNA decay by RNase E. For the sake of simplicity, the other proteins associated with the RNase E-based degradosome are not shown. In addition, this model is independent of whether RNase E is associated with the inner membrane of . 5′ monophosphate RNA, a preferred substrate for RNase E, is degraded via a 5′-end-dependent pathway. In contrast, 5′ triphosphate RNA is degraded via an RNase E internal entry mechanism. Any endonucleolytically cleaved fragments with strong secondary structures, such as one containing a Rho-independent transcription terminator shown here, undergo polyadenylation by PAP I. Subsequently, all decay intermediates are degraded by 3′→5′ exonucleases (PNPase, RNase II, and RNase R) followed by oligoribonuclease to mononucleotides. Figure is not drawn to scale. p, phosphomonoester; ppp, triphosphate.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0011-2017
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Image of FIGURE 3
FIGURE 3

Diagrammatic representation of four independent pathways of tRNA processing. (A) Processing of the polycistronic operon. RNase E initiates processing by cleaving the polycistronic transcript to release pre-tRNAs ( 11 ). Processing at the 5′ termini is carried out by RNase P. Maturation of the 3′ termini is usually carried out by RNase T and/or RNase PH. If these two enzymes are not present, RNase D and/or RNase BN can complete the process. (B) Processing of the monocistronic transcript ( 51 ). The Rho-independent transcription terminator is removed exonucleolytically by PNPase. In the absence of PNPase, a combination of RNase P and RNase II can digest the terminator. Subsequently, RNase P matures the 5′ terminus, while RNase T and RNase PH complete the process at the 3′ terminus. (C) Processing of the polycistronic operon ( 67 ). RNase P separates and pre-tRNAs by cleaving at their respective mature 5′ ends, while PNPase and RNase II shorten the 3′ Rho-dependent terminator. Subsequently, 3′→5′ exonucleases (RNase T/RNase PH/RNase D/RNase BN) mature the 3′ ends. (D). Processing of the monocistronic transcript ( 63 ). RNase E removes the Rho-independent transcription terminator to generate the mature 3′ terminus without the need of any of the 3′→5′ exonucleases. RNase P cleaves at the mature 5′ end. Figure is not drawn to scale.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0011-2017
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Image of FIGURE 4
FIGURE 4

Processing of rRNA operons in . The and operons are shown as model operons. RNase III (RIII) cleaves the 30S rRNA transcript first within the double-stranded stems formed by the spacer sequences adjacent to the mature 16S and 23S rRNAs, generating 17S, 25S, and 9S pre-rRNAs. The functional mature 16S rRNA is generated from 17S pre-rRNA after initial RNase E (E) cleavage, followed by RNase G (G) at the mature (M) 5′ end and removal of an extra 33 nucleotides at the 3′ ends by YbeY (Y) along with multiple exoribonucleases (not shown). A p5S precursor is generated from the 9S precursor by initial RNase E cleavage at 3 nucleotides upstream (E) and downstream (E) of the mature termini of the mature 5S rRNA. The mature 5′ ends of the tRNAs are generated by RNase P (P) cleavage. Exoribonucleases (X) (primarily RNase T) are responsible for the 3′ end maturation of the tRNAs, 23S rRNA, and 5S rRNA, but the RNase(s) (?) responsible for the maturation of the 5′ ends of 23S and 5S rRNAs remain unidentified. The model is not drawn to scale.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0011-2017
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Tables

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TABLE 1

Proteins involved in posttranscriptional RNA metabolism in

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.RWR-0011-2017

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