Temperature Change Induces the Expression of vuuA Encoding Vulnibactin Receptor and crp Encoding Cyclic AMP Receptor Protein in Vibrio vulnificus

Kim, Choon-Mee; Ahn, Young‐Joon; Kim, Seong-Jung; Yoon, Dae-Heung; Shin, Sung‐Heui

doi:10.1007/s00284-016-1026-8

Cited by 9 publications

(12 citation statements)

References 45 publications

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“…Accordingly, fabR, a repressor of unsaturated fatty acid metabolism was downregulated at 37 • C. Finally, we found some genes involved in vulnibactin siderophore biosynthesis and iron transport (either ferrous or ferric iron), including the plasmid gene ftbp, upregulated at all the infective temperatures ( Table 2). In accordance, crp (cyclic AMP [c-AMP] receptor protein) was upregulated at 28 and 37 • C, a regulator reported to be responsible for positive control of iron uptake systems (Choi et al, 2006;Oh et al, 2009;Kim et al, 2016). Altogether, our results show that an increase in temperature leads to a metabolic shift as it is suggested by the upregulation of multiple genes involved in biosynthesis, degradation and transport of amino acids, fatty acids, lipids and iron, which would ensure bacterial growth and constitute an advantage for V. vulnificus at host physiological temperature during the infection.…”

Section: Transcriptomic Resultsmentioning

confidence: 76%

“…Although temperaturedependent gene expression has been widely studied in other bacterial species (Gao et al, 2006;Wang et al, 2017;Matanza and Osorio, 2018;Lages et al, 2019), to our knowledge this is the first time that the global transcriptomic response to an increase in the environmental temperature is analyzed in V. vulnificus. Nevertheless, it is well known that temperature impacts V. vulnificus growth ability (Kim Y. W. et al, 2012) and the expression of some virulence factors such as the major protease (Vvp), iron uptake systems (HupA and VuuA) and quorum sensing (McDougald et al, 2001;Oh et al, 2009;Kim et al, 2016;Elgaml and Miyoshi, 2017).…”

Section: Introductionmentioning

confidence: 99%

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The Effect of the Environmental Temperature on the Adaptation to Host in the Zoonotic Pathogen Vibrio vulnificus

et al. 2020

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Vibrio vulnificus is a zoonotic pathogen that lives in temperate, tropical and subtropical aquatic ecosystems whose geographical distribution is expanding due to global warming. The species is genetically variable and only the strains that belong to the zoonotic clonal-complex can cause vibriosis in both humans and fish (being its main host the eel). Interestingly, the severity of the vibriosis in the eel and the human depends largely on the water temperature (highly virulent at 28 • C, avirulent at 20 • C or below) and on the iron content in the blood, respectively. The objective of this work was to unravel the role of temperature in the adaptation to the host through a transcriptomic and phenotypic approach. To this end, we obtained the transcriptome of a zoonotic strain grown in a minimum medium (CM9) at 20, 25, 28, and 37 • C, and confirmed the transcriptomic results by RT-qPCR and phenotypic tests. In addition, we compared the temperature stimulon with those previously obtained for iron and serum (from eel and human, respectively). Our results suggest that warm temperatures activate adaptive traits that would prepare the bacteria for host colonization (metabolism, motility, chemotaxis, and the protease activity) and fish septicemia (iron-uptake from transferrin and production of O-antigen of high molecular weight) in a generalized manner, while environmental iron controls the expression of a host-adapted virulent phenotype (toxins and the production of a protective envelope). Finally, our results confirm that beyond the effect of temperature on the V. vulnificus distribution in the environment, it also has an effect on the infectious capability of this pathogen that must be taken into account to predict the real risk of V. vulnificus infection caused by global warming.

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Section: Transcriptomic Resultsmentioning

confidence: 76%

Section: Introductionmentioning

confidence: 99%

The Effect of the Environmental Temperature on the Adaptation to Host in the Zoonotic Pathogen Vibrio vulnificus

et al. 2020

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“…; Kim et al. ). Lower temperatures can also trigger virulence, as is the case in Vibrio salmonicida (Colquhoun and Sørum ).…”

Section: Temperature Stress and Vibrionaceaementioning

confidence: 98%

“…Elevated temperatures prompt the expression of several virulence factors in the coral pathogen Vibrio coralliilyticus (Kimes et al 2012). Higher temperatures are also known to stimulate virulence in Vibrio alginolyticus, Vibrio parahaemolyticus, and Vibrio vulnificus (Mahoney et al 2010;Gu et al 2016;Kim et al 2016). Lower temperatures can also trigger virulence, as is the case in Vibrio salmonicida (Colquhoun and Sørum 2001).…”

mentioning

confidence: 99%

Adaptation to temperature stress by Vibrio fischeri facilitates this microbe's symbiosis with the Hawaiian bobtail squid ( Euprymna scolopes )

et al. 2019

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For microorganisms cycling between free‐living and host‐associated stages, where reproduction occurs in both of these lifestyles, an interesting inquiry is whether adaptation to stress during the free‐living stage can impact microbial fitness in the host. To address this topic, the mutualism between the Hawaiian bobtail squid (Euprymna scolopes) and the marine bioluminescent bacterium Vibrio fischeri was utilized. Using microbial experimental evolution, V. fischeri was selected to low (8°C), high (34°C), and fluctuating temperature stress (8°C/34°C) for 2000 generations. The temperatures 8°C and 34°C were the lower and upper growth limits, respectively. V. fischeri was also selected to benign temperatures (21°C and 28°C) for 2000 generations, which served as controls. V. fischeri demonstrated significant adaptation to low, high, and fluctuating temperature stress. V. fischeri did not display significant adaptation to the benign temperatures. Adaptation to stressful temperatures facilitated V. fischeri’s ability to colonize the squid host relative to the ancestral lines. Bioluminescence levels also increased. Evolution to benign temperatures did not manifest these results. In summary, microbial adaptation to stress during the free‐living stage can promote coevolution between hosts and microorganisms.

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“…While known for its role during catabolite repression and regulation of the lac operon, it is now appreciated that Crp regulates expression of other genes, including factors important during infection to connect changes in glucose availability to regulation of bacterial behaviors. Across γ-proteobacteria, Crp regulates biofilm formation (12,13), capsule production (14), the DNA damage response (15), toxin production (16,17), luminescence (18), and iron acquisition (19).…”

Section: Introductionmentioning

confidence: 99%

The Cyclic AMP Receptor Protein Regulates Quorum Sensing and Global Gene Expression in Yersinia pestis During Planktonic Growth and Growth in Biofilms

Ritzert

Minasov

Embry

et al. 2019

Preprint

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Cyclic adenosine monophosphate (cAMP) receptor protein (Crp) is an important transcriptional regulator of Yersinia pestis. Expression of crp increases during pneumonic plague as the pathogen depletes glucose and forms large biofilms within lungs. To better understand control of Y. pestis Crp, we determined a 1.8 Å crystal structure of the protein-cAMP complex. We found that compared to Escherichia coli Crp, C helix amino acid substitutions in Y. pestis Crp did not impact cAMP dependency of Crp to bind DNA promoters. To investigate Y. pestis Crp-regulated genes during plague pneumonia, we performed RNA-sequencing on both wild-type and ∆crp mutant bacteria growing in planktonic and biofilm states in minimal media with glucose or glycerol. Y.pestis Crp is found to dramatically alter expression of hundreds of genes dependent upon carbon source and growth state. Gel shift assays confirmed direct regulation of the malT and ptsG promoters and Crp was then linked to Y. pestis growth on maltose as a sole carbon source. Ironregulation genes ybtA and fyuA were found to be indirectly regulated by Crp. A new connection between carbon source and quorum sensing was revealed as Crp was found to regulate production of acyl-homoserine lactones (AHLs) through direct and indirect regulation of genes for AHL synthetases and receptors. AHLs were subsequently identified in the lungs of Y. pestis infected mice when crp expression is highest in Y. pestis biofilms. Thus, in addition to well-studied pla, other Crp-regulated genes likely have important functions during plague infection. IMPORTANCE Bacterial pathogens have evolved extensive signaling pathways to translate environmental signals into changes in gene expression. While Crp has long been appreciated for its role in regulating metabolism of carbon sources in many bacterial species, transcriptional profiling has revealed that this protein regulates many other aspects of bacterial physiology. The 3 plague pathogen, Y. pestis, requires this global regulator to survive in blood, skin, and lungs.During disease progression, this organism adapts to changes within these niches. In addition to regulating genes for metabolism of non-glucose sugars, we find the Crp regulates genes for virulence, metal acquisition and quorum sensing by direct or indirect mechanisms. Thus, this single transcriptional regulator, that responds to changes in available carbon sources, can regulate multiple critical behaviors for causing disease.

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Temperature Change Induces the Expression of vuuA Encoding Vulnibactin Receptor and crp Encoding Cyclic AMP Receptor Protein in Vibrio vulnificus

Cited by 9 publications

References 45 publications

The Effect of the Environmental Temperature on the Adaptation to Host in the Zoonotic Pathogen Vibrio vulnificus

The Effect of the Environmental Temperature on the Adaptation to Host in the Zoonotic Pathogen Vibrio vulnificus

Adaptation to temperature stress by Vibrio fischeri facilitates this microbe's symbiosis with the Hawaiian bobtail squid ( Euprymna scolopes )

The Cyclic AMP Receptor Protein Regulates Quorum Sensing and Global Gene Expression in Yersinia pestis During Planktonic Growth and Growth in Biofilms

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