Chapter 13 : Small Regulatory RNAs in the Enterobacterial Response to Envelope Damage and Oxidative Stress

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One major paradigm for RNA-based regulation in both eukaryotes and prokaryotes is small regulatory RNAs (sRNAs) that pair with mRNAs, leading to changes in translation and mRNA stability. In bacteria, rather than the highly processed very short microRNAs found in eukaryotes, these sRNAs are generally on the order of 50 to 200 nucleotides (nt) long, and in the Gram-negative organisms that are the major focus of this review, annealing of sRNAs to their target mRNAs is usually dependent on the RNA chaperone, Hfq. Annealing can lead to positive regulation of translation, by remodeling inhibitory RNA structures or blocking access of negative regulators (for instance, RNases or the Rho transcription termination factor), or negative regulation, by inhibiting translation, recruiting RNases, or both. A given sRNA can have multiple targets, and can carry out both negative and positive regulation ( ).

Citation: Fröhlich K, Gottesman S. 2019. Small Regulatory RNAs in the Enterobacterial Response to Envelope Damage and Oxidative Stress, p 213-228. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0022-2018
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Figure 1

Activity of sRNAs in the general stress response. (A) Together with Hfq, the sRNAs DsrA, ArcZ, and RprA activate translation of the transcript by alleviating a self-inhibitory structure within the 5′ UTR of the mRNA. The sRNA OxyS functions as an indirect, negative regulator of expression. The major alternative sigma factor RpoS governs the general stress response and controls >400 genes in and related enterobacteria, including at least four sRNAs (SdsR, SdsN, GadY, and SraL). (B) Transcription factors which are restricted to function as either activators or repressors utilize sRNAs to facilitate opposite regulation.

Citation: Fröhlich K, Gottesman S. 2019. Small Regulatory RNAs in the Enterobacterial Response to Envelope Damage and Oxidative Stress, p 213-228. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0022-2018
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Figure 2

The role of sRNAs in the major envelope stress responses. Gram-negative bacteria are diderm, with the OM and IM being separated by the periplasmic space containing the PG cell wall. (A) OM homeostasis is regulated by the RpoE response. A series of proteolysis steps results in the degradation of the anti-sigma factor RseA and concomitant release of RpoE. The large regulon of the alternative sigma factor also comprises at least three sRNAs: MicA and RybB function to downregulate the transcripts of all major OMPs to reduce the accumulation of misfolded porins within the periplasm. MicL specifically represses translation of the mRNA. (B) Maintenance of the IM relies on the CpxA-CpxR TCS, which amongst other targets controls expression of at least three sRNAs, CyaR, RprA, and CpxQ. CpxQ is a stable fragment released by RNase E processing from the 3′ end of the mRNA. In association with Hfq, CpxQ functions to repress translation of several transcripts including mRNA, which encodes a periplasmic chaperone promoting the mistargeting of OMPs into the IM. (C) The IM-associated histidine kinase RcsC, phosphotransfer protein RcsD, and response regulator RcsB constitute the core of the Rcs system. The sRNA RprA is one highly induced component of the Rcs response, which is activated by LPS damage and perturbations of the cell wall. While acting as a negative regulator of the mRNA, RprA also promotes translation of both the and the messages. As transcription of (encoding an inhibitor of the conjugation machinery) is dependent on RpoS, RprA functions at the heart of a posttranscriptional feedforward loop for RicI activity.

Citation: Fröhlich K, Gottesman S. 2019. Small Regulatory RNAs in the Enterobacterial Response to Envelope Damage and Oxidative Stress, p 213-228. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0022-2018
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Figure 3

Posttranscriptional regulation of LPS modification. The PhoQ-PhoP TCS, a major determinant of LPS modifications, is activated in response to Mg starvation as well as by AMPs. Translation of the bicistronic transcript is repressed by two sRNAs, MicA and GcvB. PhoQ-PhoP controls expression of MgrR, which, together with ArcZ, inhibits phosphoethanolamine (PEA) addition to the LPS oligosaccharide core by EptB. Both GcvB and MgrR are regulated at the posttranscriptional level by the sRNA SroC, which acts as a sponge and induces decay of its target sRNAs. Downregulation of mRNA by MicF decreases lipid A deacylation.

Citation: Fröhlich K, Gottesman S. 2019. Small Regulatory RNAs in the Enterobacterial Response to Envelope Damage and Oxidative Stress, p 213-228. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0022-2018
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Figure 4

The OxyS and MicF sRNAs are integrated into the enterobacterial response to oxidative stress. OxyS, induced by the hydrogen peroxide-responsive OxyR, downregulates mRNA (encoding a transcription factor regulating formate metabolism) and indirectly represses expression. In addition, OxyS-mediated repression of results in increased expression of , encoded in the cryptic Rac prophage. KilR sequesters FtsZ, thereby leading to inhibition of cell division and growth arrest, which allows the cell to facilitate DNA damage repair. MicF contributes to increased bacterial resistance against antibiotics of different classes by repressing the major porin OmpF. Additional targets of MicF include mRNA (encoding an LPS modification enzyme), as well as mRNA (encoding a transcriptional regulator of amino acid metabolism and transport). Expression of MicF is positively controlled by the transcription factors OmpR, MarA, Rob, and SoxS, with the last being induced in the presence of superoxide.

Citation: Fröhlich K, Gottesman S. 2019. Small Regulatory RNAs in the Enterobacterial Response to Envelope Damage and Oxidative Stress, p 213-228. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0022-2018
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