The VC1777–VC1779 proteins are members of a sialic acid-specific subfamily of TRAP transporters (SiaPQM) and constitute the sole route of sialic acid uptake in the human pathogen Vibrio cholerae

Chowdhury, Nityananda; Norris, Jessica; McAlister, Erin V.; Lau, Sze Yi; Thomas, Gavin H.; Boyd, E. Fidelma

doi:10.1099/mic.0.059659-0

Cited by 27 publications

(51 citation statements)

References 53 publications

(70 reference statements)

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“…It was recently reported that SiaPQM is a Na + -dependent sialic acid-specific TRAP transporter [21], [22]. Consistent with this, multiple genes encoding enzymes in the sialic acid utilization pathway, which convert sialic acid to fructose 6-phosphate, and neuraminidase, which convert host cell surface polysialogangliosides to GM1 monoganglioside and release sialic acid [23], were also down-regulated in the Δ nqrA-F mutant (Table 2).…”

Section: Resultssupporting

confidence: 70%

“…Given that Na + -NQR and sialic acid catabolic pathways are essential for V. cholerae colonization in the small intestine of mice [11], [24], such decreased expression of genes in the sialic acid utilization pathway might explain why the Δ nqrA-F mutant showed defects in colonization in the small intestine of mice. The dctMQP genes were recently shown to encode a C4-dicarboxylate-specific TRAP transporter and to be partly responsible for V. cholerae C4-dicarboxylates, succinate, malate and fumarate, utilization [21]. Thus, it might be possible that the decreased utilization of succinate, malate and fumarate by the V. cholerae Δ nqrA-F mutant [10] was simply caused by the decreased uptakes of these C4-dicarboxylates.…”

Section: Resultsmentioning

confidence: 99%

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Roles of the Sodium-Translocating NADH:Quinone Oxidoreductase (Na+-NQR) on Vibrio cholerae Metabolism, Motility and Osmotic Stress Resistance

et al. 2014

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The Na+ translocating NADH:quinone oxidoreductase (Na+-NQR) is a unique respiratory enzyme catalyzing the electron transfer from NADH to quinone coupled with the translocation of sodium ions across the membrane. Typically, Vibrio spp., including Vibrio cholerae, have this enzyme but lack the proton-pumping NADH:ubiquinone oxidoreductase (Complex I). Thus, Na+-NQR should significantly contribute to multiple aspects of V. cholerae physiology; however, no detailed characterization of this aspect has been reported so far. In this study, we broadly investigated the effects of loss of Na+-NQR on V. cholerae physiology by using Phenotype Microarray (Biolog), transcriptome and metabolomics analyses. We found that the V. cholerae ΔnqrA-F mutant showed multiple defects in metabolism detected by Phenotype Microarray. Transcriptome analysis revealed that the V. cholerae ΔnqrA-F mutant up-regulates 31 genes and down-regulates 55 genes in both early and mid-growth phases. The most up-regulated genes included the cadA and cadB genes, encoding a lysine decarboxylase and a lysine/cadaverine antiporter, respectively. Increased CadAB activity was further suggested by the metabolomics analysis. The down-regulated genes include sialic acid catabolism genes. Metabolomic analysis also suggested increased reductive pathway of TCA cycle and decreased purine metabolism in the V. cholerae ΔnqrA-F mutant. Lack of Na+-NQR did not affect any of the Na+ pumping-related phenotypes of V. cholerae suggesting that other secondary Na+ pump(s) can compensate for Na+ pumping activity of Na+-NQR. Overall, our study provides important insights into the contribution of Na+-NQR to V. cholerae physiology.

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Section: Resultssupporting

confidence: 70%

Section: Resultsmentioning

confidence: 99%

Roles of the Sodium-Translocating NADH:Quinone Oxidoreductase (Na+-NQR) on Vibrio cholerae Metabolism, Motility and Osmotic Stress Resistance

et al. 2014

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“…Previous studies have shown that transport of sialic acid into bacterial cells can be achieved by ABC transport systems, as seen in Haemophilus ducreyi (68), transporters of the major facilitator superfamily of proteins, as in E. coli (28,69) and Bt. fragilis (31) and/or tripartite ATP-independent periplasmic transporters, as seen first in Haemophilus influenzae (70) and in V. cholerae (71). ABC transport systems have previously been shown to be involved in carbohydrate uptake in B. breve UCC2003 (10,12,13,72).…”

Section: Discussionmentioning

confidence: 99%

Metabolism of Sialic Acid by Bifidobacterium breve UCC2003

Egan

Motherway

Ventura

et al. 2014

Appl Environ Microbiol

138

128

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bBifidobacteria constitute a specific group of commensal bacteria that inhabit the gastrointestinal tracts of humans and other mammals. Bifidobacterium breve UCC2003 has previously been shown to utilize several plant-derived carbohydrates that include cellodextrins, starch, and galactan. In the present study, we investigated the ability of this strain to utilize the mucin-and human milk oligosaccharide (HMO)-derived carbohydrate sialic acid. Using a combination of transcriptomic and functional genomic approaches, we identified a gene cluster dedicated to the uptake and metabolism of sialic acid. Furthermore, we demonstrate that B. breve UCC2003 can cross feed on sialic acid derived from the metabolism of 3=-sialyllactose, an abundant HMO, by another infant gut bifidobacterial strain, Bifidobacterium bifidum PRL2010.

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“…Besides penetrating the mucus lining, products of mucin or mucous surfaces can serve as a C source. This was shown recently (15), whereby the uptake system for sialic acids was identified in V. cholerae and found to be encoded on the Vibrio pathogenicity island. Within the host, major changes in V. cholerae gene expression take place, whereby virulence gene regulation plays a central role in controlling several regulatory cycles and numerous genes (16).…”

mentioning

confidence: 96%

Characterizing the Hexose-6-Phosphate Transport System of Vibrio cholerae, a Utilization System for Carbon and Phosphate Sources

et al. 2013

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The facultative human pathogen Vibrio cholerae transits between the gastrointestinal tract of its host and aquatic reservoirs. V. cholerae adapts to different situations by the timely coordinated expression of genes during its life cycle. We recently identified a subclass of genes that are induced at late stages of infection. Initial characterization demonstrated that some of these genes facilitate the transition of V. cholerae from host to environmental conditions. Among these genes are uptake systems lacking detailed characterization or correct annotation. In this study, we comprehensively investigated the function of the VCA0682-to-VCA0687 gene cluster, which was previously identified as in vivo induced. The results presented here demonstrate that the operon encompassing open reading frames VCA0685 to VCA0687 encodes an ABC transport system for hexose-6-phosphates with K m values ranging from 0.275 to 1.273 M for glucose-6P and fructose-6P, respectively. Expression of the operon is induced by the presence of hexose-6P controlled by the transcriptional activator VCA0682, representing a UhpA homolog. Finally, we provide evidence that the operon is essential for the utilization of hexose-6P as a C and P source. Thereby, a physiological role can be assigned to hexose-6P uptake, which correlates with increased fitness of V. cholerae after a transition from the host into phosphate-limiting environments.T he life cycle of the facultative human pathogen Vibrio cholerae is marked by repetitive transitions between aquatic environments and the host gastrointestinal tract. Besides many other variable conditions, V. cholerae has to adjust to different qualities and quantities of nutrient sources. This variability is emphasized by the fact that utilization of nutrients under laboratory conditions, such as in full broth or a chemically defined minimal medium, represents no growth limitation for clinical V. cholerae isolates (1).In the open sea, bacteria such as V. cholerae face C, N, and P limitation and are restricted to limited nutrients on a picomolar or nanomolar scale, whereby substrates become available and accessible only in specific habitats (2). Therefore, marine bacteria are found close to organic particles ranging from micrometer-to millimeter-sized aggregates. These organic particles derive from different sources, such as lysed or dead phytoplankton, zooplankton, or fecal pellets. They deliver organic and inorganic substrates in concentrations that are up to 4 orders of magnitude greater than those found in particle-free open seawater (for a recent review, see reference 2). Therefore, many plants and animals in the ocean serve as microbial niches for V. cholerae (3-6). For example, copepods or other crustaceans contain or are covered with chitin, a ␤,1-4-linked polymer of 2-acetamido-2-deoxy-␤-D-glucopyranoside (GlcNAc) n and its deacetylated form, chitosan. These substrates are utilized by Vibrio sp. as C and N sources (7-9). In addition, biofilm formation on chitinous surfaces plays a crucial role in V. choler...

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The VC1777–VC1779 proteins are members of a sialic acid-specific subfamily of TRAP transporters (SiaPQM) and constitute the sole route of sialic acid uptake in the human pathogen Vibrio cholerae

Cited by 27 publications

References 53 publications

Roles of the Sodium-Translocating NADH:Quinone Oxidoreductase (Na+-NQR) on Vibrio cholerae Metabolism, Motility and Osmotic Stress Resistance

Roles of the Sodium-Translocating NADH:Quinone Oxidoreductase (Na+-NQR) on Vibrio cholerae Metabolism, Motility and Osmotic Stress Resistance

Metabolism of Sialic Acid by Bifidobacterium breve UCC2003

Characterizing the Hexose-6-Phosphate Transport System of Vibrio cholerae, a Utilization System for Carbon and Phosphate Sources

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