Niche adaptation limits bacteriophage predation of Vibrio cholerae in a nutrient-poor aquatic environment

Vibrio cholerae, the causative agent of cholera, has reservoirs in fresh and brackish water where it interacts with virulent bacteriophages. Phages are the most abundant biological entity on earth and coevolve with bacteria. It was reported that concentrations of phage and V. cholerae inversely correlate in aquatic reservoirs and in the human small intestine, and therefore that phages may quench cholera outbreaks. Although there is strong evidence for phage predation in cholera patients, evidence is lacking for phage predation of V. cholerae in aquatic environments. Here, we used three virulent phages, ICP1, ICP2, and ICP3, commonly shed by cholera patients in Bangladesh, as models to understand the predation dynamics in microcosms simulating aquatic environments. None of the phages were capable of predation in fresh water, and only ICP1 was able to prey on V. cholerae in estuarine water due to a requirement for salt. We conclude that ICP2 and ICP3 are better adapted for predation in a nutrient rich environment. Our results point to the evolution of niche-specific predation by V. cholerae-specific virulent phages, which complicates their use in predicting or monitoring cholera outbreaks as well as their potential use in reducing aquatic reservoirs of V. cholerae in endemic areas.

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Niche adaptation limits bacteriophage predation of Vibrio cholerae in a nutrient-poor aquatic environment

10.1101/492439 ◽

2018 ◽

Author(s):

Cecilia A. Silva-Valenzuela ◽

Andrew Camilli

Keyword(s):

Vibrio Cholerae ◽

Direct Evidence ◽

Biological Entity ◽

Aquatic Environments ◽

Natural Setting ◽

Aquatic Microcosms ◽

Human Small Intestine ◽

Niche Adaptation ◽

Adaptation Limits ◽

Potential Use

AbstractVibrio cholerae, the causative agent of cholera, has reservoirs in fresh and brackish water where it interacts with virulent bacteriophages. Phages are the most abundant biological entity on earth and co-evolve with bacteria. It was reported that concentrations of phage and V. cholerae inversely correlate in aquatic reservoirs and in the human small intestine, and therefore that phages may quench cholera outbreaks. Although there is strong evidence for phage predation in cholera patients, evidence is lacking for phage predation of V. cholerae in aquatic environments. Here, we used three virulent phages, ICP1, ICP2, and ICP3, commonly shed by cholera patients in Bangladesh, as models to understand the predation dynamics in microcosms simulating aquatic environments. None of the phages were capable of predation in fresh water, and only ICP1 was able to prey on V. cholerae in estuarine water due to a requirement for salt. We conclude that ICP2 and ICP3 are better adapted for predation in a nutrient rich environment. Our results point to the evolution of niche-specific predation by V. cholerae-specific virulent phages, which complicates their use in predicting or monitoring cholera outbreaks as well as their potential use in reducing aquatic reservoirs of V. cholerae in endemic areas.Significance statementVirulent phages can reduce populations of bacteria and help shape bacterial evolution. Here, we used three virulent phages to understand their equilibrium with V. cholerae in nutrient-limiting aquatic microcosms. It has been proposed that phages quench cholera outbreaks, but no direct evidence of phage predation in aquatic environments had been established. Here we show that different phages possess varied abilities to infect in certain niches or stages of the host bacterial life cycle. Unveiling the phage/bacterial interactions in their natural setting is important to the understanding of cholera outbreaks and could be ultimately used to help develop a method for outbreak prediction and/or control.

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Vibrio cholerae O1 adherence to villi and lymphoid follicle epithelium: in vitro model using formalin-treated human small intestine and correlation between adherence and cell-associated hemagglutinin levels.

Infection and Immunity ◽

10.1128/iai.56.12.3241-3250.1988 ◽

1988 ◽

Vol 56 (12) ◽

pp. 3241-3250 ◽

Cited By ~ 25

Author(s):

T Yamamoto ◽

T Kamano ◽

M Uchimura ◽

M Iwanaga ◽

T Yokota

Keyword(s):

Small Intestine ◽

Vibrio Cholerae ◽

In Vitro Model ◽

Lymphoid Follicle ◽

Human Small Intestine ◽

Vibrio Cholerae O1 ◽

Vitro Model

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Faculty Opinions recommendation of Niche adaptation limits bacteriophage predation of Vibrio cholerae in a nutrient-poor aquatic environment.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.734849355.793558878 ◽

2019 ◽

Author(s):

Chris Waters

Keyword(s):

Vibrio Cholerae ◽

Aquatic Environment ◽

Niche Adaptation ◽

Adaptation Limits

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Alkaline pH increases swimming speed and facilitates mucus penetration for Vibrio cholerae

Journal of Bacteriology ◽

10.1128/jb.00607-20 ◽

2021 ◽

Author(s):

Nguyen T. Q. Nhu ◽

John S. Lee ◽

Helen J. Wang ◽

Yann S. Dufour

Keyword(s):

Small Intestine ◽

Vibrio Cholerae ◽

Swimming Speed ◽

Cell Tracking ◽

Alkaline Ph ◽

Flagellar Motility ◽

Human Small Intestine ◽

Intestinal Mucus ◽

Mucus Penetration ◽

El Tor

Intestinal mucus is the first line of defense against intestinal pathogens. It acts as a physical barrier between epithelial tissues and the lumen that enteropathogens must overcome to establish a successful infection. We investigated the motile behavior of two V. cholerae strains (El Tor C6706 and Classical O395) in mucus using single cell tracking in unprocessed porcine intestinal mucus. We determined that V. cholerae is able to penetrate mucus using flagellar motility and that alkaline pH increases swimming speed, and consequently, improves mucus penetration. Microrheological measurements indicate that changes in pH between 6 and 8 (the physiological range for the human small intestine) had little effect on the viscoelastic properties of mucus. Finally, we determined that acidic pH promotes surface attachment by activating the mannose-sensitive haemagglutinin (MshA) pilus in V. cholerae El Tor C6706 without a measurable change in the total cellular concentration of the secondary messenger cyclic dimeric guanosine monophosphate (c-di-GMP). Overall, our results support that pH is an important factor affecting the motile behavior of V. cholerae and its ability to penetrate mucus. Therefore, changes in pH along the human small intestine may play a role in determining the preferred site for V. cholerae during infection. IMPORTANCE The diarrheal disease cholera is still a burden for populations in developing countries with poor sanitation. To develop effective vaccines and prevention strategies against Vibrio cholerae, we must understand the initial steps of infection leading to the colonization of the small intestine. To infect the host and deliver the cholera toxin, V. cholerae has to penetrate the mucus layer protecting the intestinal tissues. However, the interaction of V. cholerae with intestinal mucus has not been extensively investigated. In this report, we demonstrated using single cell tracking that V. cholerae is able to penetrate intestinal mucus using flagellar motility. In addition, we observed that alkaline pH improves the ability of V. cholerae to penetrate mucus. This finding has important implications for understanding the dynamics of infection because pH varies significantly along the small intestine, between individuals, and between species. Blocking mucus penetration by interfering with flagellar motility in V. cholerae, reinforcing the mucosa, controlling intestinal pH, or manipulating the intestinal microbiome, will offer new strategies to fight cholera.

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Electron microscopic study of Vibrio cholerae O1 adherence to the mucus coat and villus surface in the human small intestine.

Infection and Immunity ◽

10.1128/iai.56.10.2753-2759.1988 ◽

1988 ◽

Vol 56 (10) ◽

pp. 2753-2759 ◽

Cited By ~ 33

Author(s):

T Yamamoto ◽

T Yokota

Keyword(s):

Small Intestine ◽

Vibrio Cholerae ◽

Microscopic Study ◽

Electron Microscopic Study ◽

Electron Microscopic ◽

Human Small Intestine ◽

Vibrio Cholerae O1

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Electron probe x-ray microanalysis and electron microscopy of amino acid absorption and transport by the small intestine: inhibition by chemical poisons and correlation to the elemental composition of the epithelial cells

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100142311 ◽

1986 ◽

Vol 44 ◽

pp. 134-135

Author(s):

A. J. Tousimis

Keyword(s):

Small Intestine ◽

Amino Acid ◽

Epithelial Cells ◽

Elemental Composition ◽

Isotope Labeling ◽

Structural Components ◽

X Ray ◽

Human Small Intestine ◽

Transport Studies

The elemental composition of amino acids is similar to that of the major structural components of the epithelial cells of the small intestine and other tissues. Therefore, their subcellular localization and concentration measurements are not possible by x-ray microanalysis. Radioactive isotope labeling: I131-tyrosine, Se75-methionine and S35-methionine have been successfully employed in numerous absorption and transport studies. The latter two have been utilized both in vitro and vivo, with similar results in the hamster and human small intestine. Non-radioactive Selenomethionine, since its absorption/transport behavior is assumed to be the same as that of Se75- methionine and S75-methionine could serve as a compound tracer for this amino acid.

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