Cra negatively regulates acid survival in Yersinia pseudotuberculosis

Hu, Yangbo; Lu, Pei Jung; Zhang, Yong; Li, Yunlong; Li, Lamei; Huang, Li; Chen, Shiyun

doi:10.1111/j.1574-6968.2011.02227.x

Cited by 8 publications

(11 citation statements)

References 23 publications

(36 reference statements)

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“…While the cra gene (originally designated fruR) is adjacent to the fructose operon fruBKA in Pseudomonas putida (43), this gene (B1H58_03575) lies far away from fruBKA (B1H58_14040 to B1H58_14050) in P. alhagi LTYR-11Z, in line with members of enteric bacteria, such as E. coli and Yersinia pseudotuberculosis (43,44,59). It has been reported that carbon nutrition influences colonization and maintenance of pathogenic and commensal E. coli strains in the mouse intestine (60)(61)(62), while the pathogenic EHEC O157:H7 strain required gluconeogenic nutrients to successfully colonize the intestines precolonized with the commensal E. coli Nissle 1917 (63).…”

Section: Discussionmentioning

confidence: 99%

The Catabolite Repressor/Activator Cra Is a Bridge Connecting Carbon Metabolism and Host Colonization in the Plant Drought Resistance-Promoting Bacterium Pantoea alhagi LTYR-11Z

Zhang

Chen

et al. 2018

Appl Environ Microbiol

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Efficient root colonization is a prerequisite for application of plant growth promoting (PGP) bacteria in improving health and yield of agricultural crops. We have recently identified an endophytic bacterium LTYR-11Z with multiple PGP properties that effectively colonizes the root system of wheat and improves its growth and drought tolerance. To identify novel regulatory genes required for wheat colonization, we screened a LTYR-11Z transposon (Tn) insertion library and found to be a colonization-related gene. By using RNA-seq analysis, we found that transcriptional levels of an operon, the gene encoding an anti-FlhDC factor and the gene encoding an enzyme for synthesis of cyclic dimeric GMP (c-di-GMP) were significantly downregulated in the mutant Δ Further studies demonstrated that Cra directly binds to the promoters of the operon, and and activates their expression, thus inhibiting motility and promoting exopolysaccharides (EPS) production and biofilm formation. Consistent with previous findings that Cra plays a role in transcriptional regulation in response to carbon source availability, the activating effects of Cra were much more pronounced when LTYR-11Z was grown within a gluconeogenic environment than when it was grown within a glycolytic environment. We further demonstrate that the ability of LTYR-11Z to colonize wheat roots is modulated by the availability of carbon sources. All together, these results uncover a novel strategy utilized by LTYR-11Z to achieve host colonization in response to carbon nutrition in the environment, in which Cra bridges a connection between carbon metabolism and colonization capacity of LTYR-11Z. Rapid and appropriate response to environmental signals is crucial for bacteria to adapt to competitive environments and to establish interactions with their hosts. Efficient colonization and persistence within the host is controlled by various regulatory factors that respond to specific environmental cues. The most common is nutrient availability. In this work, we unraveled the pivotal role of Cra in regulation of colonization ability of LTYR-11Z in response to carbon source availability. Moreover, we identified three novel members of the Cra regulon involved in EPS synthesis, regulation of flagellar biosynthesis, and synthesis of c-di-GMP, and propose a working model to explain the Cra-mediated regulatory mechanism that links carbon metabolism to host colonization. This study elucidates the regulatory role of Cra in bacterial attachment and colonization of plants, which raises the possibility to extend our studies to other bacteria associated with plant and human health.

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Section: Discussionmentioning

confidence: 99%

The Catabolite Repressor/Activator Cra Is a Bridge Connecting Carbon Metabolism and Host Colonization in the Plant Drought Resistance-Promoting Bacterium Pantoea alhagi LTYR-11Z

Zhang

Chen

et al. 2018

Appl Environ Microbiol

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“…Stingl and De Reuse (2005) have reported that Y. pseudotuberculosis uses urease (UreABC) to convert urea to ammonia that neutralizes H + for acid tolerance. Recently, Hu et al have shown that the regulator Cra negatively regulates acid tolerance in Y. pseudotuberculosis (Hu et al, 2011). Recently, Hu et al have shown that the regulator Cra negatively regulates acid tolerance in Y. pseudotuberculosis (Hu et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…A Y. pseudotuberculosis enzyme involved in aspartate metabolism (AspA) also plays a role in acid survival (Hu et al, 2010). Recently, Hu et al have shown that the regulator Cra negatively regulates acid tolerance in Y. pseudotuberculosis (Hu et al, 2011). In addition, two-component regulon assays have revealed that several regulators, including PhoP, OmpR and PmrA, control acid survival in Y. pseudotuberculosis (Flamez et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

A type VI secretion system regulated by OmpR in Yersinia pseudotuberculosis functions to maintain intracellular pH homeostasis

Zhang

Wang

Song

et al. 2012

Environmental Microbiology

120

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Type VI secretion systems (T6SSs) which widely distributed in Gram-negative bacteria have been primarily studied in the context of cell interactions with eukaryotic hosts or other bacteria. We have recently identified a thermoregulated T6SS4 in the enteric pathogen Yersinia pseudotuberculosis. Here we report that OmpR directly binds to the promoter of T6SS4 operon and regulates its expression. Further, we observed that the OmpR-regulated T6SS4 is essential for bacterial survival under acidic conditions and that its expression is induced by low pH. Moreover, we showed that T6SS4 plays a role in pumping H(+) out of the cell to maintain intracellular pH homeostasis. The acid tolerance phenotype of T6SS4 is dependent on the ATPase activity of ClpV4, one of the components of T6SS4. These results not only uncover a novel strategy utilized by Y. pseudotuberculosis for acid resistance, but also reveal that T6SS, a bacteria secretion system known to be functional in protein transportation has an unexpected function in H(+) extrusion under acid conditions.

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“…Other bacterial factors that promote survival under acidic conditions include urease [126], TatC [127], PhoP, OmpR, and PmrA [128, 129]. Acidic pH also induces a downregulation of the transcriptional regulator, Cra (for catabolite repressor/activator), which increases bacterial acid survival [130]. Presumably Cra mediates this action via transcriptional regulation, but its mechanism of action remains unknown.…”

Section: Introductionmentioning

confidence: 99%

Pathogenesis ofY. enterocoliticaandY. pseudotuberculosisin Human Yersiniosis

Galindo

Rosenzweig

Kirtley

et al. 2011

Journal of Pathogens

158

103

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Yersiniosis is a food-borne illness that has become more prevalent in recent years due to human transmission via the fecal-oral route and prevalence in farm animals. Yersiniosis is primarily caused by Yersinia enterocolitica and less frequently by Yersinia pseudotuberculosis. Infection is usually characterized by a self-limiting acute infection beginning in the intestine and spreading to the mesenteric lymph nodes. However, more serious infections and chronic conditions can also occur, particularly in immunocompromised individuals. Y. enterocolitica and Y. pseudotuberculosis are both heterogeneous organisms that vary considerably in their degrees of pathogenicity, although some generalizations can be ascribed to pathogenic variants. Adhesion molecules and a type III secretion system are critical for the establishment and progression of infection. Additionally, host innate and adaptive immune responses are both required for yersiniae clearance. Despite the ubiquity of enteric Yersinia species and their association as important causes of food poisoning world-wide, few national enteric pathogen surveillance programs include the yersiniae as notifiable pathogens. Moreover, no standard exists whereby identification and reporting systems can be effectively compared and global trends developed. This review discusses yersinial virulence factors, mechanisms of infection, and host responses in addition to the current state of surveillance, detection, and prevention of yersiniosis.

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Cra negatively regulates acid survival in Yersinia pseudotuberculosis

Cited by 8 publications

References 23 publications

The Catabolite Repressor/Activator Cra Is a Bridge Connecting Carbon Metabolism and Host Colonization in the Plant Drought Resistance-Promoting Bacterium Pantoea alhagi LTYR-11Z

The Catabolite Repressor/Activator Cra Is a Bridge Connecting Carbon Metabolism and Host Colonization in the Plant Drought Resistance-Promoting Bacterium Pantoea alhagi LTYR-11Z

A type VI secretion system regulated by OmpR in Yersinia pseudotuberculosis functions to maintain intracellular pH homeostasis

Pathogenesis ofY. enterocoliticaandY. pseudotuberculosisin Human Yersiniosis

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