Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs

Reddi, Geethika; Pruss, Kali M.; Cottingham, Kathryn L.; Taylor, Ronald K.; Almagro‐Moreno, Salvador

doi:10.1371/journal.pone.0201383

Cited by 30 publications

(31 citation statements)

References 55 publications

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“…Consistent with this notion, depletion of sialic acid (Neu5Ac) transporters (encoded in VC1777-1779) attenuates colonization [69]. During this process, V. cholerae needs to overcome a number of challenges such as acid stress, antimicrobial peptides, host immune response, and SCFAs [64,66,68]. The reduction of intestinal SCFAs in patients with diarrhea and recovery of normal SCFA levels after conventional treatment support that the SCFAs could be a contributing factor to eubiosis of the intestinal microbiota [70].…”

Section: Discussionmentioning

confidence: 85%

“…When the pathogen enters the intestinal tract, the next strategy for its proliferation is to colonize the epithelial cells covered with a viscous layer of mucus. V. cholerae effectively responds to the mucus glycan and catabolize the polysaccharides to acquire competitive advantage in host intestine [65][66][67][68]. Glucosamine-6-phosphate (GlcNP-6), a common intermediate molecule shared between the catabolic pathways of GlcNAc and Neu5Ac, was reported to be indispensable for V. cholerae motility [68].…”

Section: Discussionmentioning

confidence: 99%

“…V. cholerae effectively responds to the mucus glycan and catabolize the polysaccharides to acquire competitive advantage in host intestine [65][66][67][68]. Glucosamine-6-phosphate (GlcNP-6), a common intermediate molecule shared between the catabolic pathways of GlcNAc and Neu5Ac, was reported to be indispensable for V. cholerae motility [68]. Chemotaxis mediated by motility toward the nutrient sources is important for colonization and proliferation of V. cholerae [68].…”

Section: Discussionmentioning

confidence: 99%

“…Glucosamine-6-phosphate (GlcNP-6), a common intermediate molecule shared between the catabolic pathways of GlcNAc and Neu5Ac, was reported to be indispensable for V. cholerae motility [68]. Chemotaxis mediated by motility toward the nutrient sources is important for colonization and proliferation of V. cholerae [68].…”

Section: Discussionmentioning

confidence: 99%

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Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine

et al. 2019

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Background Recent evidence suggests that the commensal microbes act as a barrier against invading pathogens and enteric infections are the consequences of multi-layered interactions among commensals, pathogens, and the host intestinal tissue. However, it remains unclear how perturbations of the gut microbiota compromise host infection resistance, especially through changes at species and metabolite levels. Results Here, we illustrate how Bacteroides vulgatus, a dominant species of the Bacteroidetes phylum in mouse intestine, suppresses infection by Vibrio cholerae, an important human pathogen. Clindamycin (CL) is an antibiotic that selectively kills anaerobic bacteria, and accordingly Bacteroidetes are completely eradicated from CL-treated mouse intestines. The Bacteroidetes-depleted adult mice developed severe cholera-like symptoms, when infected with V. cholerae. Germ-free mice mono-associated with B. vulgatus became resistant to V. cholerae infection. Levels of V. cholerae growth-inhibitory metabolites including short-chain fatty acids plummeted upon CL treatment, while levels of compounds that enhance V. cholerae proliferation were elevated. Furthermore, the intestinal colonization process of V. cholerae was well-simulated in CL-treated adult mice. Conclusions Overall, we provide insights into how a symbiotic microbe and a pathogenic intruder interact inside host intestine. We identified B. vulgatus as an indigenous microbial species that can suppress intestinal infection. Our results also demonstrate that commensal-derived metabolites are a critical determinant for host resistance against V. cholerae infection, and that CL pretreatment of adult mice generates a simple yet useful model of cholera infection.

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Section: Discussionmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Commensal-derived metabolites govern Vibrio cholerae pathogenesis in host intestine

et al. 2019

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“…Previous studies have shown that Vibrio species can utilize intestinal mucus as a carbon and energy source (25)(26)(27)(28). Therefore, we examined the expression pattern of the ula genes in V. cholerae cells growth in M9-Mucus.…”

Section: Resultsmentioning

confidence: 99%

L-ascorbic acid (vitamin C) fermentation by the human pathogenVibrio cholerae

Rosenberger

McDonald

Boyd

2020

Preprint

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L-ascorbic acid, commonly known as vitamin C, is a ubiquitous 6-carbon carbohydrate characterized by its ability to scavenge free radicals. In enteric bacteria, L-ascorbate can be utilized as a nutrient using the UlaABCDEF and UlaG-UlaRpathway under anaerobic conditions. In this study, we identified homologs of the Ula system within Vibrio cholerae and showed that V. cholerae is able to utilize L-ascorbate as an energy source. Growth pattern assays of a ulaG in-frame deletion mutant demonstrated that ulaG is essential for L-ascorbate fermentation. Expression analysis showed that ula catabolism and transport genes were significantly induced in cells grown in the presence of L-ascorbate compared to glucose and these genes were also highly induced during growth on intestinal mucus. In in vitro growth competition assays, the ulaG mutant was outcompeted by wild type when grown in intestinal mucus suggesting the Ula system could be important for fitness. Within the ula operon in V. cholerae and all Vibrio species a homology of ORF VCA0243 is present that encodes a pyridoxal phosphate (PLP) phosphatase. This enzyme in E. coli, converts the active form of vitamin B6 PLP to its inactive form pyridoxal (PL). In V. splendidus and related species, the aerobic and anaerobic L-ascorbate pathway genes cluster together and both systems contain a PLP phosphatase. An in-frame deletion mutant of vca0243 resulted in a growth defect in L-ascorbate fermentation as well as additional carbon and amino acid sources indicating a role in cellular metabolism. Phylogenetic analysis of UlaG and UlaD suggested the region was acquired by horizontal gene transfer.ImportanceL-ascorbate is a carbohydrate present in the human intestine, available for microbial consumption and several enteric species have been shown to utilize this compound as an energy source. We demonstrated that L-ascorbate fermentation genes are also present among marine bacteria from the family Vibrionaceae and that the human pathogen V. cholerae can ferment L-ascorbate as an energy source. Within the Ula operon in all Vibrionaceae, a putative pyridoxal phosphate phosphatase was present that was required for L-ascorbate fermentation and cellular metabolism in general. The Ula system was present among a limited number of genera within Vibrionaceae; Vibrio, Aliivibrio and Photobacterium and showed an evolutionary history consistent with horizontal transfer between genera and species.

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