<i>Staphylococcus aureus</i> RNAIII and Its Regulon Link Quorum Sensing, Stress Responses, Metabolic Adaptation, and Regulation of Virulence Gene Expression

Bronesky, Delphine; Wu, Zongfu; Marzi, Stefano; Walter, P.; Geissmann, Thomas; Moreau, Karen; Vandenesch, François; Caldelari, Isabelle; Romby, Pascale

doi:10.1146/annurev-micro-102215-095708

Cited by 178 publications

(150 citation statements)

References 132 publications

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“…While mRNAs were expected to accumulate in the pellet together with actively translating ribosomes (Supplementary Figure S1A), sRNAs were not ( Figure 1F (87)). Moreover, ribosome association of sRNAs can hint at a dual function of an RNA, as first describe for Staphylococcus aureus RNAIII, which is both a regulatory RNA and the mRNA of -hemolysin (88). Here, we observed SgrS-the best-characterized dualfunction RNA of E. coli (89)-almost exclusively in the pellet fraction ( Figure 1F).…”

Section: Discussionsupporting

confidence: 74%

Grad-seq shines light on unrecognized RNA and protein complexes in the model bacteriumEscherichia coli

Hör

Giorgio

Gerovac

et al. 2020

Preprint

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ABSTRACTStable protein complexes, including those formed with RNA, are major building blocks of every living cell. Escherichia coli has been the leading bacterial organism with respect to global protein-protein networks. Yet, there has been no global census of RNA/protein complexes in this model species of microbiology. Here, we performed Grad-seq to establish an RNA/protein complexome, reconstructing sedimentation profiles in a glycerol gradient for ~85% of all E. coli transcripts and ~49% of the proteins. These include the majority of small noncoding RNAs (sRNAs) detectable in this bacterium as well as the general sRNA-binding proteins, CsrA, Hfq and ProQ. In presenting use cases for utilization of these RNA and protein maps, we show that a stable association of RyeG with 30S ribosomes gives this seemingly noncoding RNA of prophage origin away as an mRNA of a toxic small protein. Similarly, we show that the broadly conserved uncharacterized protein YggL is a 50S subunit factor in assembled 70S ribosomes. Overall, this study crucially extends our knowledge about the cellular interactome of the primary model bacterium E. coli through providing global RNA/protein complexome information and should facilitate functional discovery in this and related species.

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Section: Discussionsupporting

confidence: 74%

Grad-seq shines light on unrecognized RNA and protein complexes in the model bacteriumEscherichia coli

Hör

Giorgio

Gerovac

et al. 2020

Preprint

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“…The presentation of the anti-Shine Dalgarno sequence by a pyrimidine-rich loop is reminiscent of how CyaR sRNA recognizes the ompX mRNA in E. coli and Salmonella (106–108). Moreover, target recognition via pyrimidine-rich loops is a hallmark of regulatory sRNAs in Staphylococcus aureus which generally work without Hfq (109). Similar to these latter sRNAs, RcoF1/2 likely undergo a structural rearrangement as they recognize the prpB mRNA, as best visible in the structure probing experiment with RcoF1/2 (Figure 8B).…”

Section: Discussionmentioning

confidence: 99%

The primary transcriptome of Neisseria meningitidis and its interaction with the RNA chaperone Hfq

Heidrich

Bauriedl

Barquist

et al. 2017

Nucleic Acids Research

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Neisseria meningitidis is a human commensal that can also cause life-threatening meningitis and septicemia. Despite growing evidence for RNA-based regulation in meningococci, their transcriptome structure and output of regulatory small RNAs (sRNAs) are incompletely understood. Using dRNA-seq, we have mapped at single-nucleotide resolution the primary transcriptome of N. meningitidis strain 8013. Annotation of 1625 transcriptional start sites defines transcription units for most protein-coding genes but also reveals a paucity of classical σ70-type promoters, suggesting the existence of activators that compensate for the lack of −35 consensus sequences in N. meningitidis. The transcriptome maps also reveal 65 candidate sRNAs, a third of which were validated by northern blot analysis. Immunoprecipitation with the RNA chaperone Hfq drafts an unexpectedly large post-transcriptional regulatory network in this organism, comprising 23 sRNAs and hundreds of potential mRNA targets. Based on this data, using a newly developed gfp reporter system we validate an Hfq-dependent mRNA repression of the putative colonization factor PrpB by the two trans-acting sRNAs RcoF1/2. Our genome-wide RNA compendium will allow for a better understanding of meningococcal transcriptome organization and riboregulation with implications for colonization of the human nasopharynx.

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“…The QS Agr system present in the Staphylococci is well studied on the molecular level (12)(13)(14)(15). The system is composed of AgrA, AgrB, AgrC, and AgrD encoded by the agrBDCA operon and the divergently transcribed RNAIII molecule (depicted in Fig.…”

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confidence: 99%

“…Phosphorylated AgrA triggers transcription of its own operon (agrBDCA) as well as the divergently transcribed regulatory RNAIII. Many extracellular virulence factors, such as hemolysins are under the control of RNAIII (15). Of note, RNAIII also encodes a small peptide, Hld (16,17).…”

mentioning

confidence: 99%

Oxidative stress drives the selection of quorum sensing mutants in the Staphylococcus aureus population

George

Hrubesch

Breuing

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Quorum sensing (QS) is the central mechanism by which social interactions within the bacterial community control bacterial behavior. QS-negative cells benefit by exploiting public goods produced by the QS-proficient population. Mechanisms to keep the balance between producers and nonproducers within the population are expected but have not been elucidated for peptide-based QS systems in gram-positive pathogens. The Agr system of Staphylococcus aureus comprises the secretion and sensing of an autoinducing peptide to activate its own expression via the response regulator AgrA as well as the expression of a regulatory RNAIII and psmα/psmß coding for phenol-soluble modulins (PSMs). Agr mutants can be monitored on blood agar due to their nonhemolytic phenotype. In vitro evolution and competition experiments show that they readily accumulate in a process that is accelerated by ciprofloxacin, while the wild type (WT) is retained in the population at low numbers. However, agr mutants possess a fitness advantage only under aerobic conditions. Under hypoxia, Agr activity is increased but without the expected fitness cost. The Agr-imposed oxygen-dependent fitness cost is not due to a metabolic burden but due to the reactive oxygen species (ROS)-inducing capacity of the PSMs and RNAIII-regulated factors. Thus, selection of mutants is dictated by the QS system itself. Under aerobic conditions, emergence of agr-negative mutants may provide the population with a fitness advantage while hypoxia favors QS maintenance and even affords increased toxin production. The oxygen-driven tuning of the Agr system might be of importance to provide the pathogen with capabilities crucial for disease progression.

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Staphylococcus aureus RNAIII and Its Regulon Link Quorum Sensing, Stress Responses, Metabolic Adaptation, and Regulation of Virulence Gene Expression

Cited by 178 publications

References 132 publications

Grad-seq shines light on unrecognized RNA and protein complexes in the model bacteriumEscherichia coli

Grad-seq shines light on unrecognized RNA and protein complexes in the model bacteriumEscherichia coli

The primary transcriptome of Neisseria meningitidis and its interaction with the RNA chaperone Hfq

Oxidative stress drives the selection of quorum sensing mutants in the Staphylococcus aureus population

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