RNase E and the High-Fidelity Orchestration of RNA Metabolism

Abstract

The bacterial endoribonuclease RNase E occupies a pivotal position in the control of gene expression, as its actions either commit transcripts to an irreversible fate of rapid destruction or unveil their hidden functions through specific processing. Moreover, the enzyme contributes to quality control of rRNAs. The activity of RNase E can be directed and modulated by signals provided through regulatory RNAs that guide the enzyme to specific transcripts that are to be silenced. Early in its evolutionary history, RNase E acquired a natively unfolded appendage that recruits accessory proteins and RNA. These accessory factors facilitate the activity of RNase E and include helicases that remodel RNA and RNA-protein complexes, and polynucleotide phosphorylase, a relative of the archaeal and eukaryotic exosomes. RNase E also associates with enzymes from central metabolism, such as enolase and aconitase. RNase E-based complexes are diverse in composition, but generally bear mechanistic parallels with eukaryotic machinery involved in RNA-induced gene regulation and transcript quality control. That these similar processes arose independently underscores the universality of RNA-based regulation in life. Here we provide a synopsis and perspective of the contributions made by RNase E to sustain robust gene regulation with speed and accuracy.

RNase III-mediated processing of atrans-acting bacterial sRNA and itscis-encoded antagonist

“…Considering sRNA biogenesis, RNase E has the most well-characterized role in bacteria (Miyakoshi et al, 2015a;Bandyra & Luisi, 2018) but is absent in ~1/5 sequenced strains (Hui et al, 2014). Despite its broader conservation, understanding of the role of RNase III in sRNA biogenesis lags behind that of RNase E. However, genome-wide surveys in diverse bacteria have identified many potential sRNAs as RNase III targets that remain to be studied (DiChiara et al, 2016;Stead et al, 2011;Altuvia et al, 2018;Lioliou et al, 2012Lioliou et al, , 2013Le Rhun et al, 2017;Gatewood et al, 2012;Lybecker et al, 2014;Vogel et al, 2003), suggesting that the role of RNase III in sRNA biogenesis might be larger than previously appreciated.…”

RNase E and HupB dynamics foster mycobacterial cell homeostasis and fitness

“…The strongest correlations were found between RNase E and constituents of the RNA degradosome ( Figures 3 C and 3D), with the translation initiation factor InfA ( Figure 3 E), with the DNA repair enzyme UvrA ( Figure 3 F), and with the stress-response proteins Obg ( Kumar et al., 2017 ) and Lsr2 ( Figures 3 I and 3J). In summary, the combination of proteomic and single-cell analyses pointed to possible interactions of RNase E with known and unknown members of the RNA degradosome ( Bandyra et al., 2018 ; Płociński et al., 2019 ), and with proteins involved in critical aspects of mycobacterial cell physiology. Further analysis will be required to determine whether these potential interactions are direct or indirect, and whether they have a functional role in cellular adaptation to changing environmental conditions.…”

LcrQ Coordinates with the YopD-LcrH Complex To Repress lcrF Expression and Control Type III Secretion by Yersinia pseudotuberculosis

“…For example, the basis of our Drne strain is an incomplete deletion caused by a 39 truncation of the rne gene (36). It is evident that the nature of the rne mutation, coupled to the expression of other RNases in the organism, can affect the phenotypes displayed by rne mutants with respect to RNA degradosome assembly, mRNA turnover, maturation of rRNA and tRNA precursors, processing and degradation of regulatory RNAs, as well as rRNA quality control (45). Any of these situations may be at play in our Yersinia Drne background.…”