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Role of RNA Decay in Bacterial Gene Regulation

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: 20 December 2024 | Viewed by 3992

Special Issue Editors


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Guest Editor
Academia Sinica, Institute of Molecular Biology, Taipei, Taiwan
Interests: RNA decay

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Guest Editor
Department of Immunology, Microbiology and Parasitology, Faculty of Science and Technology, University of the Basque Country, Barrio Sarriena, S/N, 48940 Leioa, Spain
Interests: bacterial stress responses; post-transcriptional control; small regulatory RNAs; RNA processing and decay; Escherichia coli; ecology of Vibrio species
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Special Issue Information

Dear Colleagues,

The marked ability of microorganisms to rapidly adapt to changing environments is largely rooted in their capacity to promptly reprogram gene expression by synthesizing new coding mRNAs, along with the concomitant elimination of redundant transcripts. The rapid and selective elimination of redundant bacterial transcripts is conducted by diverse mRNA decay machineries, the main components of which have been well characterized for a few model organisms including Escherichia coli and Bacillus subtilis. Various studies of mRNA decay mechanisms have shown that the 5′ phosphorylation status, nucleotide composition, and structure of individual mRNAs can greatly impact mRNA turnover, and they have revealed a number of cis-acting regulatory elements located within the 5′- and 3′ end regions. Some important cis-acting elements include 5′ stabilizers, riboswitches, repetitive extragenic palindromic sequences, and 3′ poly(A) tails, which regulate the accessibility of individual transcripts (or their segments) to different ribonucleases and regulatory factors. In addition to cis-acting elements, a number of trans-acting factors (e.g., small regulatory RNAs (sRNAs) and ribosomes) are likewise known for their essential roles in controlling RNA turnover under numerous stress conditions.

The major aim of this Special Issue is to draw attention to recent progress in the field, and, more specifically, to update the reader about (i) new RNA degradation mechanisms; (ii) the role of cis- and trans-acting mRNA stability determinants; and (iii) the multifaceted characteristics of RNA decay machineries, such as their diverse composition, biological functions, mechanisms of action, and phylogenetic conservation. Accordingly, we wish to invite prospective authors to submit original research and review articles focused on fundamental and applied aspects of RNA turnover in bacteria.

Potential topics include, but are not limited to, the following:

  • Advanced experimental approaches for monitoring the abundance and fate of RNA molecules.
  • Regulation of mRNA stability by cis-acting elements (RNA stabilizers, riboswitches, and polyadenylation).
  • Control of mRNA stability by small regulatory RNAs.
  • Interdependence of translation and mRNA decay.
  • Ribonucleases involved in RNA turnover and their ancillary factors.

Dr. Sue Lin-Chao
Prof. Dr. Vladimir Kaberdin
Guest Editors

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Keywords

  • RNA stabilizers
  • RNA decay
  • RNA turnover
  • small regulatory RNAs
  • post-transcriptional control

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Published Papers (4 papers)

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Research

16 pages, 19868 KiB  
Article
Kinetic Features of Degradation of R-Loops by RNase H1 from Escherichia coli
by Aleksandra A. Kuznetsova, Iurii A. Kosarev, Nadezhda A. Timofeyeva, Darya S. Novopashina and Nikita A. Kuznetsov
Int. J. Mol. Sci. 2024, 25(22), 12263; https://doi.org/10.3390/ijms252212263 - 15 Nov 2024
Viewed by 394
Abstract
R-loops can act as replication fork barriers, creating transcription–replication collisions and inducing replication stress by arresting DNA synthesis, thereby possibly causing aberrant processing and the formation of DNA strand breaks. RNase H1 (RH1) is one of the enzymes that participates in R-loop degradation [...] Read more.
R-loops can act as replication fork barriers, creating transcription–replication collisions and inducing replication stress by arresting DNA synthesis, thereby possibly causing aberrant processing and the formation of DNA strand breaks. RNase H1 (RH1) is one of the enzymes that participates in R-loop degradation by cleaving the RNA strand within a hybrid RNA–DNA duplex. In this study, the kinetic features of the interaction of RH1 from Escherichia coli with R-loops of various structures were investigated. It was found that the values of the dissociation constants Kd were minimal for complexes of RH1 with model R-loops containing a 10–11-nt RNA–DNA hybrid part, indicating effective binding. Analysis of the kinetics of RNA degradation in the R-loops by RH1 revealed that the rate-limiting step of the process was catalytic-complex formation. In the presence of RNA polymerase, the R-loops containing a ≤16-nt RNA–DNA hybrid part were efficiently protected from cleavage by RH1. In contrast, R-loops containing longer RNA–DNA hybrid parts, as a model of an abnormal transcription process, were not protected by RNA polymerase and were effectively digested by RH1. Full article
(This article belongs to the Special Issue Role of RNA Decay in Bacterial Gene Regulation)
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17 pages, 1648 KiB  
Article
Membrane Localization of RNase Y Is Important for Global Gene Expression in Bacillus subtilis
by Soumaya Laalami, Marina Cavaiuolo, Jacques Oberto and Harald Putzer
Int. J. Mol. Sci. 2024, 25(15), 8537; https://doi.org/10.3390/ijms25158537 - 5 Aug 2024
Viewed by 789
Abstract
RNase Y is a key endoribonuclease that regulates global mRNA turnover and processing in Bacillus subtilis and likely many other bacteria. This enzyme is anchored to the cell membrane, creating a pseudo-compartmentalization that aligns with its role in initiating the decay of mRNAs [...] Read more.
RNase Y is a key endoribonuclease that regulates global mRNA turnover and processing in Bacillus subtilis and likely many other bacteria. This enzyme is anchored to the cell membrane, creating a pseudo-compartmentalization that aligns with its role in initiating the decay of mRNAs primarily translated at the cell periphery. However, the reasons behind and the consequences of RNase Y’s membrane attachment remain largely unknown. In our study, we examined a strain expressing wild-type levels of a cytoplasmic form of RNase Y from its chromosomal locus. This strain exhibits a slow-growth phenotype, similar to that of an RNase Y null mutant. Genome-wide data reveal a significant impact on the expression of hundreds of genes. While certain RNA substrates clearly depend on RNase Y’s membrane attachment, others do not. We observed no correlation between mRNA stabilization in the mutant strains and the cellular location or function of the encoded proteins. Interestingly, the Y-complex, a specificity factor for RNase Y, also appears also recognize the cytoplasmic form of the enzyme, restoring wild-type levels of the corresponding transcripts. We propose that membrane attachment of RNase Y is crucial for its functional interaction with many coding and non-coding RNAs, limiting the cleavage of specific substrates, and potentially avoiding unfavorable competition with other ribonucleases like RNase J, which shares a similar evolutionarily conserved cleavage specificity. Full article
(This article belongs to the Special Issue Role of RNA Decay in Bacterial Gene Regulation)
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13 pages, 3427 KiB  
Article
Identification of Ribonuclease Inhibitors for the Control of Pathogenic Bacteria
by Rute G. Matos, Katie J. Simmons, Colin W. G. Fishwick, Kenneth J. McDowall and Cecília M. Arraiano
Int. J. Mol. Sci. 2024, 25(15), 8048; https://doi.org/10.3390/ijms25158048 - 24 Jul 2024
Viewed by 924
Abstract
Bacteria are known to be constantly adapting to become resistant to antibiotics. Currently, efficient antibacterial compounds are still available; however, it is only a matter of time until these compounds also become inefficient. Ribonucleases are the enzymes responsible for the maturation and degradation [...] Read more.
Bacteria are known to be constantly adapting to become resistant to antibiotics. Currently, efficient antibacterial compounds are still available; however, it is only a matter of time until these compounds also become inefficient. Ribonucleases are the enzymes responsible for the maturation and degradation of RNA molecules, and many of them are essential for microbial survival. Members of the PNPase and RNase II families of exoribonucleases have been implicated in virulence in many pathogens and, as such, are valid targets for the development of new antibacterials. In this paper, we describe the use of virtual high-throughput screening (vHTS) to identify chemical compounds predicted to bind to the active sites within the known structures of RNase II and PNPase from Escherichia coli. The subsequent in vitro screening identified compounds that inhibited the activity of these exoribonucleases, with some also affecting cell viability, thereby providing proof of principle for utilizing the known structures of these enzymes in the pursuit of new antibacterials. Full article
(This article belongs to the Special Issue Role of RNA Decay in Bacterial Gene Regulation)
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23 pages, 2063 KiB  
Article
Hfq-Antisense RNA I Binding Regulates RNase E-Dependent RNA Stability and ColE1 Plasmid Copy Number
by Wei-Syuan Wang and Sue Lin-Chao
Int. J. Mol. Sci. 2024, 25(7), 3955; https://doi.org/10.3390/ijms25073955 - 2 Apr 2024
Viewed by 1468
Abstract
The mechanisms and consequences of gene regulation by Hfq on trans-encoded small RNAs (sRNAs) have been well studied and documented. Recent employment of Genomic SELEX to search for Hfq-binding motifs has indicated that Hfq might frequently regulate gene expression controlled by cis [...] Read more.
The mechanisms and consequences of gene regulation by Hfq on trans-encoded small RNAs (sRNAs) have been well studied and documented. Recent employment of Genomic SELEX to search for Hfq-binding motifs has indicated that Hfq might frequently regulate gene expression controlled by cis-antisense RNAs. Here, we use the classic ColE1 plasmid antisense RNA-based regulation model (i.e., RNA I) to study the role of Hfq in controlling antisense regulatory functions. We show that Hfq exhibits a high binding affinity for RNA I and that binding limits RNase E cleavage, thereby stabilizing RNA I and reducing the plasmid copy number. Full-length RNA I displays a binding affinity for Hfq in the sub-micromolar range. In vivo overexpression of Hfq prolongs RNA I stability and reduces the ColE1 plasmid copy number, whereas deletion of hfq reduces RNA I stability and increases the plasmid copy number. RNA I predominantly binds to the proximal face of Hfq and exhibits competitive ability against a chromosome-borne proximal face-bound sRNA (DsrA) for Hfq binding. Through its strong promoter and high gene dosage features, plasmid-encoded antisense RNA I results in high RNA I expression, so it may antagonize the effects of trans-encoded RNAs in controlling target gene expression. Full article
(This article belongs to the Special Issue Role of RNA Decay in Bacterial Gene Regulation)
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