The Vibrio vulnificus stressosome is an oxygen-sensor involved in regulating iron metabolism

Heinz, Veronika; Jäckel, Wenke; Kaltwasser, Susann; Cutugno, Laura; Bedrunka, Patricia; Graf, Anica; Reder, Alexander; Michalik, Stephan; Dhople, Vishnu M.; Madej, M. Gregor; Conway, Maria; Lechner, Marcus; Riedel, Katharina; Bange, Gert; Boyd, Aoife; Völker, Uwe; Lewis, Richard J.; Marles‐Wright, Jon; Ziegler, Christine; Pané‐Farré, Jan

doi:10.1038/s42003-022-03548-w

Cited by 8 publications

(21 citation statements)

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“…vulnificus in the environment and for survival during the infection process. For this reason, this work focused on characterization of the in vivo role of the stressosome in this marine pathogen during growth in rich media, to complement the previous studies in chemically defined minimal media [28]. This characterization confirmed that the stressosome genes are transcribed in LB+2.5 % NaCl (LBN), a rich media commonly used to culture this bacterium, and focused on the effects of the stressosome on the growth and stress response of V.…”

Section: Introductionmentioning

confidence: 66%

“…We confirmed that there were no growth differences between the ΔRSTX mutant and the wild-type in the absence of stress, as expected, and focused on the effects of hypoxia and high temperature stresses on growth. Differences between the two strains did not emerge and the effects of hypoxia and high temperature were comparable between the two strains, despite the hypothesized role of the stressosome as an oxygen sensor [28], thus highlighting the media-specific role of the stressosome in V. vulnificus .…”

Section: Discussionmentioning

confidence: 99%

“…The use of rifampicin-resistant V. vulnificus has been previously employed [34,35] to counter-select the donor strain after conjugation. pDS_ΔRSBRSTX carries the knockout allele with a deletion from nucleotide 4 of VvrsbR to nucleotide 577 of VvrsbX in the pDS132 suicide vector [28,30,36,37]. Biparental conjugations with E. coli SM10λpir (pDS_ΔRSBRSTX) were performed to introduce the allele into Rif R V. vulnificus and selection of first recombinants was performed on LBN agar containing 5 µg ml −1 chloramphenicol+50 µg ml −1 rifampicin.…”

Section: Construction Of the V Vulnificus δRstx Knock-out Mutantmentioning

confidence: 99%

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The Vibrio vulnificus stressosome is dispensable in nutrient-rich media

Cutugno

Cafferty

Pané‐Farré

et al. 2023

Access Microbiology

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The stressosome is a protein complex that senses environmental stresses and mediates the stress response in several Gram-positive bacteria through the activation of the alternative sigma factor SigB. The stressosome locus is found in 44 % of Gram-negative Vibrio vulnificus isolates. However, V. vulnificus does not possess SigB. Nonetheless, in nutrient-limited media, the stressosome modulates gene transcription and bacterial behaviour. In this work, the expression of the stressosome genes was proven during stationary phase in nutrient-rich media and co-transcription as one operonic unit of the stressosome locus and its putative downstream regulatory locus was demonstrated. The construction of a stressosome mutant lacking the genes encoding the four proteins constituting the stressosome complex (VvRsbR, VvRsbS, VvRsbT, VvRsbX) allowed us to examine the role of this complex in vivo. Extensive phenotypic characterization of the ΔRSTX mutant in nutrient-rich media showed that the stressosome does not contribute to growth of V. vulnificus . Moreover, the stressosome did not modulate the tolerance or survival response of V. vulnificus to the range of stresses tested, which included ethanol, hyperosmolarity, hypoxia, high temperature, acidity and oxidative stress. Furthermore, the stressosome was dispensable for motility and exoenzyme production of V. vulnificus in nutrient-rich media. Therefore, in conclusion, although stressosome gene transcription occurs in nutrient-rich media, the stressosome neither has an essential role in stress responses of V. vulnificus nor does it seem to modulate these activities in these conditions. We hypothesise that the stressosome is expressed in nutrient-rich conditions as a sensor complex, but that activation of the complex does not occur in this environment.

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Section: Introductionmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Section: Construction Of the V Vulnificus δRstx Knock-out Mutantmentioning

confidence: 99%

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The Vibrio vulnificus stressosome is dispensable in nutrient-rich media

Cutugno

Cafferty

Pané‐Farré

et al. 2023

Access Microbiology

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“…The two‐component system within che2 comprises a serine phosphatase response regulator (RsbU) and an anti‐anti‐sigma factor (RsbV) (Figure 1b ). In various Vibrio species, these are involved in O 2 ‐dependent stress responses and in regulating iron metabolism (Heinz et al, 2022 ; Jia et al, 2016 ). We investigated potential interactions between the CheA2 histidine kinase and the RsbU response regulator using a bacterial two‐hybrid assay, but observed no CheA2‐RsbU interactions (data not shown).…”

Section: Resultsmentioning

confidence: 99%

The Aer2 chemoreceptor from Vibrio vulnificus is a tri‐PAS‐heme oxygen sensor

Stuffle

Suzuki

Orillard

et al. 2022

Molecular Microbiology

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The marine pathogen Vibrio vulnificus senses and responds to environmental stimuli via two chemosensory systems and 42–53 chemoreceptors. Here, we present an analysis of the V. vulnificus Aer2 chemoreceptor, VvAer2, which is the first V. vulnificus chemoreceptor to be characterized. VvAer2 is related to the Aer2 receptors of other gammaproteobacteria, but uncharacteristically contains three PAS domains (PAS1‐3), rather than one or two. Using an E. coli chemotaxis hijack assay, we determined that VvAer2, like other Aer2 receptors, senses and responds to O2. All three VvAer2 PAS domains bound pentacoordinate b‐type heme and exhibited similar O2 affinities. PAS2 and PAS3 both stabilized O2 via conserved Iβ‐Trp residues, but PAS1, which was easily oxidized in vitro, was unaffected by Iβ‐Trp replacement. Our results support a model in which PAS1 is largely dispensable for O2‐mediated signaling, whereas PAS2 modulates PAS3 signaling, and PAS3 signals to the downstream domains. Each PAS domain appeared to be positionally optimized, because PAS swapping caused altered signaling properties, and neither PAS1 nor PAS2 could replace PAS3. Our findings strengthen previous conclusions that Aer2 receptors are O2 sensors, but with distinct N‐terminal domain arrangements that facilitate, modulate and tune responses based on environmental signals.

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“…The same holds true for the edge between V. vulnificus quantity and O 2 mean 0–0 , which has been observed elsewhere [ 65 , 66 , 67 ]. While changes in oxygen saturation can affect the metabolism of V. vulnificus [ 68 ], this edge more likely reflects the strong effects of temperature on oxygen solubility.…”

Section: Discussionmentioning

confidence: 99%

First Steps towards a near Real-Time Modelling System of Vibrio vulnificus in the Baltic Sea

Schütt

Hundsdörfer

Hoyningen-Huene

et al. 2023

IJERPH

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Over the last two decades, Vibrio vulnificus infections have emerged as an increasingly serious public health threat along the German Baltic coast. To manage related risks, near real-time (NRT) modelling of V. vulnificus quantities has often been proposed. Such models require spatially explicit input data, for example, from remote sensing or numerical model products. We tested if data from a hydrodynamic, a meteorological, and a biogeochemical model are suitable as input for an NRT model system by coupling it with field samples and assessing the models’ ability to capture known ecological parameters of V. vulnificus. We also identify the most important predictors for V. vulnificus in the Baltic Sea by leveraging the St. Nicolas House Analysis. Using a 27-year time series of sea surface temperature, we have investigated trends of V. vulnificus season length, which pinpoint hotspots mainly in the east of our study region. Our results underline the importance of water temperature and salinity on V. vulnificus abundance but also highlight the potential of air temperature, oxygen, and precipitation to serve as predictors in a statistical model, albeit their relationship with V. vulnificus may not be causal. The evaluated models cannot be used in an NRT model system due to data availability constraints, but promising alternatives are presented. The results provide a valuable basis for a future NRT model for V. vulnificus in the Baltic Sea.

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The Vibrio vulnificus stressosome is an oxygen-sensor involved in regulating iron metabolism

Cited by 8 publications

References 76 publications

The Vibrio vulnificus stressosome is dispensable in nutrient-rich media

The Vibrio vulnificus stressosome is dispensable in nutrient-rich media

The Aer2 chemoreceptor from Vibrio vulnificus is a tri‐PAS‐heme oxygen sensor

First Steps towards a near Real-Time Modelling System of Vibrio vulnificus in the Baltic Sea

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