RNA Thermometer-coordinated Assembly of the Yersinia Injectisome

Pienkoß, Stephan; Javadi, Soheila; Chaoprasid, Paweena; Holler, Marcel; Roßmanith, Johanna; Dersch, Petra; Narberhaus, Franz

doi:10.1016/j.jmb.2022.167667

Cited by 12 publications

(5 citation statements)

References 84 publications

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“…virulence factor OmpA [16], the T3SS components YscJ and YscT [17], the T3SS regulator YopN [18], and the secreted bacterial toxin CnfY [19].…”

Section: Plos Geneticsmentioning

confidence: 99%

“…LcrF is the master virulence regulator in Y. pestis and Y. pseudotuberculosis and itself is subject to stringent temperature control [11,40]. Having KatY production under tight dual temperature control is reminiscent of the situation of the T3SS genes yopN, yscT and yscJ, which are under transcriptional control by LcrF and contain their own RNATs as translational control elements [17,18].…”

Section: Plos Geneticsmentioning

confidence: 99%

“…Apart from this transcriptional regulation, global RNA structuromics approaches revealed the existence of RNATs upstream of numerous genes suggesting a contribution to sensing and responding to a warm-blooded host [ 14 , 15 ]. Several of the RNAT-regulated genes play a direct role in virulence, such as the genes for the adhesion protein AilA [ 14 ], the virulence factor OmpA [ 16 ], the T3SS components YscJ and YscT [ 17 ], the T3SS regulator YopN [ 18 ], and the secreted bacterial toxin CnfY [ 19 ].…”

Section: Introductionmentioning

confidence: 99%

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The oxidative stress response, in particular the katY gene, is temperature-regulated in Yersinia pseudotuberculosis

et al. 2023

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Pathogenic bacteria, such as Yersinia pseudotuberculosis encounter reactive oxygen species (ROS) as one of the first lines of defense in the mammalian host. In return, the bacteria react by mounting an oxidative stress response. Previous global RNA structure probing studies provided evidence for temperature-modulated RNA structures in the 5’-untranslated region (5’-UTR) of various oxidative stress response transcripts, suggesting that opening of these RNA thermometer (RNAT) structures at host-body temperature relieves translational repression. Here, we systematically analyzed the transcriptional and translational regulation of ROS defense genes by RNA-sequencing, qRT-PCR, translational reporter gene fusions, enzymatic RNA structure probing and toeprinting assays. Transcription of four ROS defense genes was upregulated at 37°C. The trxA gene is transcribed into two mRNA isoforms, of which the most abundant short one contains a functional RNAT. Biochemical assays validated temperature-responsive RNAT-like structures in the 5’-UTRs of sodB, sodC and katA. However, they barely conferred translational repression in Y. pseudotuberculosis at 25°C suggesting partially open structures available to the ribosome in the living cell. Around the translation initiation region of katY we discovered a novel, highly efficient RNAT that was primarily responsible for massive induction of KatY at 37°C. By phenotypic characterization of catalase mutants and through fluorometric real-time measurements of the redox-sensitive roGFP2-Orp1 reporter in these strains, we revealed KatA as the primary H2O2 scavenger. Consistent with the upregulation of katY, we observed an improved protection of Y. pseudotuberculosis at 37°C. Our findings suggest a multilayered regulation of the oxidative stress response in Yersinia and an important role of RNAT-controlled katY expression at host body temperature.

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“…virulence factor OmpA [16], the T3SS components YscJ and YscT [17], the T3SS regulator YopN [18], and the secreted bacterial toxin CnfY [19].…”

Section: Plos Geneticsmentioning

confidence: 99%

Section: Plos Geneticsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The oxidative stress response, in particular the katY gene, is temperature-regulated in Yersinia pseudotuberculosis

et al. 2023

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“…In bacteria, the main temperature-sensing mechanisms are RNA thermometers, which regulate the expression of genes at the post-transcriptional level through structured RNAs [ 18 ]. RNA thermometers regulate different physiological features like the virulence factor tviA in Salmonella typhi or the type three injectisome in Yersinia pseudotuberculosis [ 18 , 21 , 22 ]. Temperature-dependent traits, mainly associated with virulence, host colonization, and survival, have been recently reviewed in Pseudomonas spp., including P. aeruginosa [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo

Solar Venero,

Galeano,

Luqman

et al. 2024

BMC Biol

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Background Staphylococcus aureus (SA) and Pseudomonas aeruginosa (PA) cause a wide variety of bacterial infections and coinfections, showing a complex interaction that involves the production of different metabolites and metabolic changes. Temperature is a key factor for bacterial survival and virulence and within the host, bacteria could be exposed to an increment in temperature during fever development. We analyzed the previously unexplored effect of fever-like temperatures (39 °C) on S. aureus USA300 and P. aeruginosa PAO1 microaerobic mono- and co-cultures compared with 37 °C, by using RNAseq and physiological assays including in vivo experiments. Results In general terms both temperature and co-culturing had a strong impact on both PA and SA with the exception of the temperature response of monocultured PA. We studied metabolic and virulence changes in both species. Altered metabolic features at 39 °C included arginine biosynthesis and the periplasmic glucose oxidation in S. aureus and P. aeruginosa monocultures respectively. When PA co-cultures were exposed at 39 °C, they upregulated ethanol oxidation-related genes along with an increment in organic acid accumulation. Regarding virulence factors, monocultured SA showed an increase in the mRNA expression of the agr operon and hld, pmsα, and pmsβ genes at 39 °C. Supported by mRNA data, we performed physiological experiments and detected and increment in hemolysis, staphyloxantin production, and a decrease in biofilm formation at 39 °C. On the side of PA monocultures, we observed an increase in extracellular lipase and protease and biofilm formation at 39 °C along with a decrease in the motility in correlation with changes observed at mRNA abundance. Additionally, we assessed host–pathogen interaction both in vitro and in vivo. S. aureus monocultured at 39οC showed a decrease in cellular invasion and an increase in IL-8—but not in IL-6—production by A549 cell line. PA also decreased its cellular invasion when monocultured at 39 °C and did not induce any change in IL-8 or IL-6 production. PA strongly increased cellular invasion when co-cultured at 37 and 39 °C. Finally, we observed increased lethality in mice intranasally inoculated with S. aureus monocultures pre-incubated at 39 °C and even higher levels when inoculated with co-cultures. The bacterial burden for P. aeruginosa was higher in liver when the mice were infected with co-cultures previously incubated at 39 °C comparing with 37 °C. Conclusions Our results highlight a relevant change in the virulence of bacterial opportunistic pathogens exposed to fever-like temperatures in presence of competitors, opening new questions related to bacteria-bacteria and host–pathogen interactions and coevolution.

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“…In bacteria, the main temperature sensing mechanisms are RNA thermometers, which regulate the expression of genes at the post-transcriptional level through structured RNAs (18). Several researchers have reported that RNA thermometers regulate different physiological features like the virulence factor tviA in Salmonella typhi or the type three injectisome in Yersinia pseudotuberculosis (18,21,22)Temperature-dependent traits, mainly associated with virulence, host colonization and survival, have been recently reviewed in Pseudomonas spp., including P. aeruginosa (23).…”

Section: Introductionmentioning

confidence: 99%

Fever-like temperature impacts onStaphylococcus aureusandPseudomonas aeruginosainteraction, physiology, and virulence bothin vitroandin vivo

Venero

Galeano

Luqman

et al. 2023

Preprint

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Staphylococcus aureusandPseudomonas aeruginosaare two bacterial species that cause a wide variety of infections and coinfections. The interaction between these species is complex and involves the production of different metabolites and metabolic changes. The impact of elevated body temperature, such as fever, on the physiology and interaction of these pathogens remains poorly understood. Therefore, the aim of this work was to analyze the effect of moderate fever-like temperatures (39°C) onS. aureusUSA300 andP. aeruginosaPAO1 mono- and co-cultures in comparison with 37°C, by using RNAseq and physiological assays in microaerobiosis. Both bacterial species showed metabolic alterations in response to temperature but also in response to the competitor. Organic acid production and nitrite content in the supernatant were altered both by the presence of the competitor and the incubation temperature. Interaction ANOVA showed that, inS. aureus, gene expression presented interaction between the temperature and the presence of the competitor. Among these genes, the most relevant were theagroperon and three of its direct target genespsmβ,psmβ2andhld. In the A549 epithelial lung cell line, fever-like temperatures impacted in vitro virulence, antibiotic resistance, cell invasion, and cytokine production. In agreement with thein vitroassays, the survival of mice that had been intranasally inoculated withS. aureusmonocultures pre-incubated at 39°C showed reduced survival after 10 days. An even higher mortality of around 30% was observed in mice that had been inoculated with co-cultures pre-incubated at 39°C. The bacterial burden in the lungs, kidney, and liver was higher for both species when the mice were infected with co-cultures previously incubated at 39°C. Our results highlight a relevant change in the virulence of bacterial opportunistic pathogens exposed to fever-like temperatures, opening new questions related to bacteria-bacteria and host-pathogen interactions and coevolution.

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RNA Thermometer-coordinated Assembly of the Yersinia Injectisome

Cited by 12 publications

References 84 publications

The oxidative stress response, in particular the katY gene, is temperature-regulated in Yersinia pseudotuberculosis

The oxidative stress response, in particular the katY gene, is temperature-regulated in Yersinia pseudotuberculosis

Fever-like temperature impacts on Staphylococcus aureus and Pseudomonas aeruginosa interaction, physiology, and virulence both in vitro and in vivo

Fever-like temperature impacts onStaphylococcus aureusandPseudomonas aeruginosainteraction, physiology, and virulence bothin vitroandin vivo

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