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Impact of bacteria motility in the encounter rates with bacteriophage in mucus.

ABSTRACT: Bacteriophages-or phages-are viruses that infect bacteria and are present in large concentrations in the mucosa that cover the internal organs of animals. Immunoglobulin (Ig) domains on the phage surface interact with mucin molecules, and this has been attributed to an increase in the encounter rates of phage with bacteria in mucus. However, the physical mechanism behind this phenomenon remains unclear. A continuous time random walk (CTRW) model simulating the diffusion due to mucin-T4 phage interactions was developed and calibrated to empirical data. A Langevin stochastic method for Escherichia coli (E. coli) run-and-tumble motility was combined with the phage CTRW model to describe phage-bacteria encounter rates in mucus for different mucus concentrations. Contrary to previous theoretical analyses, the emergent subdiffusion of T4 in mucus did not enhance the encounter rate of T4 against bacteria. Instead, for static E. coli, the diffusive T4 mutant lacking Ig domains outperformed the subdiffusive T4 wild type. E. coli's motility dominated the encounter rates with both phage types in mucus. It is proposed, that the local fluid-flow generated by E. coli's motility combined with T4 interacting with mucins may be the mechanism for increasing the encounter rates between the T4 phage and E. coli bacteria.

SUBMITTER: Joiner KL

PROVIDER: S-EPMC6848219 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Impact of bacteria motility in the encounter rates with bacteriophage in mucus.

Joiner Kevin L KL Baljon Arlette A Barr Jeremy J Rohwer Forest F Luque Antoni A

Scientific reports 20191111 1

Bacteriophages-or phages-are viruses that infect bacteria and are present in large concentrations in the mucosa that cover the internal organs of animals. Immunoglobulin (Ig) domains on the phage surface interact with mucin molecules, and this has been attributed to an increase in the encounter rates of phage with bacteria in mucus. However, the physical mechanism behind this phenomenon remains unclear. A continuous time random walk (CTRW) model simulating the diffusion due to mucin-T4 phage int ...[more]

PMID: 31712565

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Project description:Metazoans were proposed to host bacteriophages on their mucosal surfaces in a symbiotic relationship, where phages provide an external immunity against bacterial infections and the metazoans provide phages a medium for interacting with bacteria. However, scarce empirical evidence and model systems have left the phage-mucus interaction poorly understood. Here, we show that phages bind both to porcine mucus and to rainbow trout (Oncorhynchus mykiss) primary mucus, persist up to 7?days in the mucosa, and provide protection against Flavobacterium columnare Also, exposure to mucus changes the bacterial phenotype by increasing bacterial virulence and susceptibility to phage infections. This trade-off in bacterial virulence reveals ecological benefit of maintaining phages in the metazoan mucosal surfaces. Tests using other phage-bacterium pairs suggest that phage binding to mucus may be widespread in the biosphere, indicating its importance for disease, ecology, and evolution. This phenomenon may have significant potential to be exploited in preventive phage therapy.IMPORTANCE The mucosal surfaces of animals are habitat for microbes, including viruses. Bacteriophages-viruses that infect bacteria-were shown to be able to bind to mucus. This may result in a symbiotic relationship in which phages find bacterial hosts to infect, protecting the mucus-producing animal from bacterial infections in the process. Here, we studied phage binding on mucus and the effect of mucin on phage-bacterium interactions. The significance of our research is in showing that phage adhesion to mucus results in preventive protection against bacterial infections, which will serve as basis for the development of prophylactic phage therapy approaches. Besides, we also reveal that exposure to mucus upregulates bacterial virulence and that this is exploited by phages for infection, adding one additional layer to the metazoan-bacterium-phage biological interactions and ecology. This phenomenon might be widespread in the biosphere and thus crucial for understanding mucosal diseases, their outcome and treatment.

Project description:Cholera disease is caused by Vibrio cholerae infecting the lining of the small intestine and results in severe diarrhea. V. cholerae's swimming motility is known to play a crucial role in pathogenicity and may aid the bacteria in crossing the intestinal mucus barrier to reach sites of infection, but the exact mechanisms are unknown. The cell can be either pushed or pulled by its single polar flagellum, but there is no consensus on the resulting repertoire of motility behaviors. We use high-throughput three-dimensional (3D) bacterial tracking to observe V. cholerae swimming in buffer, in viscous solutions of the synthetic polymer PVP, and in mucin solutions that may mimic the host environment. We perform a statistical characterization of its motility behavior on the basis of large 3D trajectory data sets. We find that V. cholerae performs asymmetric run-reverse-flick motility, consisting of a sequence of a forward run, reversal, and a shorter backward run, followed by a turn by approximately 90°, called a flick, preceding the next forward run. Unlike many run-reverse-flick swimmers, V. cholerae's backward runs are much shorter than its forward runs, resulting in an increased effective diffusivity. We also find that the swimming speed is not constant but subject to frequent decreases. The turning frequency in mucin matches that observed in buffer. Run-reverse-flick motility and speed fluctuations are present in all environments studied, suggesting that these behaviors also occur in natural aquatic habitats as well as the host environment. IMPORTANCE Cholera disease produces vomiting and severe diarrhea and causes approximately 100,000 deaths per year worldwide. The disease is caused by the bacterium Vibrio cholerae colonizing the lining of the small intestine. V. cholerae's ability to swim is known to increase its infectivity, but the underlying mechanisms are not known. One possibility is that swimming aids in crossing the protective mucus barrier that covers the lining of the small intestine. Our work characterizing how V. cholerae swims in environments that mimic properties of the host environment may advance the understanding of how motility contributes to infection.

Dataset Information

Impact of bacteria motility in the encounter rates with bacteriophage in mucus.

Publications

Impact of bacteria motility in the encounter rates with bacteriophage in mucus.

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