Genes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization

ABSTRACT During its life cycle, the facultative human pathogen Vibrio cholerae, which is the causative agent of the diarrheal disease cholera, needs to adapt to a variety of different conditions, such as the human host or the aquatic environment. Importantly, cholera infections originate from the aq...

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Autores principales: Cornelia List, Andreas Grutsch, Claudia Radler, Fatih Cakar, Franz G. Zingl, Kristina Schild-Prüfert, Stefan Schild
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:2c619c7c9bcf4073a2232b1926b0bbcf2021-11-15T15:24:23ZGenes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization10.1128/mSphereDirect.00238-182379-5042https://doaj.org/article/2c619c7c9bcf4073a2232b1926b0bbcf2018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphereDirect.00238-18https://doaj.org/toc/2379-5042ABSTRACT During its life cycle, the facultative human pathogen Vibrio cholerae, which is the causative agent of the diarrheal disease cholera, needs to adapt to a variety of different conditions, such as the human host or the aquatic environment. Importantly, cholera infections originate from the aquatic reservoir where V. cholerae persists between the outbreaks. In the aquatic environment, bacteria are constantly threatened by predatory protozoa and nematodes, but our knowledge of the response pathways and adaptation strategies of V. cholerae to such stressors is limited. Using a temporally controlled reporter system of transcription, we identified more than 100 genes of V. cholerae induced upon exposure to the nematode Caenorhabditis elegans, which emerged recently as a valuable model for environmental predation during the aquatic lifestyle of V. cholerae. Besides others, we identified and validated the genes encoding the mannose-sensitive hemagglutinin (MSHA) type IV pilus to be significantly induced upon exposure to the nematode. Subsequent analyses demonstrated that the mannose-sensitive hemagglutinin is crucial for attachment of V. cholerae in the pharynx of the worm and initiation of colonization, which results in growth retardation and developmental delay of C. elegans. Thus, the surface adhesion factor MSHA could be linked to a fitness advantage of V. cholerae upon contact with bacterium-grazing nematodes. IMPORTANCE The waterborne diarrheal disease cholera is caused by the bacterium Vibrio cholerae. The facultative human pathogen persists as a natural inhabitant in the aquatic ecosystem between outbreaks. In contrast to the human host, V. cholerae requires a different set of genes to survive in this hostile environment. For example, predatory micrograzers are commonly found in the aquatic environment and use bacteria as a nutrient source, but knowledge of the interaction between bacterivorous grazers and V. cholerae is limited. In this study, we successfully adapted a genetic reporter technology and identified more than 100 genes activated by V. cholerae upon exposure to the bacterium-grazing nematode Caenorhabditis elegans. This screen provides a first glimpse into responses and adaptational strategies of the bacterial pathogen against such natural predators. Subsequent phenotypic characterization revealed the mannose-sensitive hemagglutinin to be crucial for colonization of the worm, which causes developmental delay and growth retardation.Cornelia ListAndreas GrutschClaudia RadlerFatih CakarFranz G. ZinglKristina Schild-PrüfertStefan SchildAmerican Society for MicrobiologyarticleMSHARIVETbacterial grazingbacterivorouschitindevelopmentMicrobiologyQR1-502ENmSphere, Vol 3, Iss 3 (2018)
institution DOAJ
collection DOAJ
language EN
topic MSHA
RIVET
bacterial grazing
bacterivorous
chitin
development
Microbiology
QR1-502
spellingShingle MSHA
RIVET
bacterial grazing
bacterivorous
chitin
development
Microbiology
QR1-502
Cornelia List
Andreas Grutsch
Claudia Radler
Fatih Cakar
Franz G. Zingl
Kristina Schild-Prüfert
Stefan Schild
Genes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization
description ABSTRACT During its life cycle, the facultative human pathogen Vibrio cholerae, which is the causative agent of the diarrheal disease cholera, needs to adapt to a variety of different conditions, such as the human host or the aquatic environment. Importantly, cholera infections originate from the aquatic reservoir where V. cholerae persists between the outbreaks. In the aquatic environment, bacteria are constantly threatened by predatory protozoa and nematodes, but our knowledge of the response pathways and adaptation strategies of V. cholerae to such stressors is limited. Using a temporally controlled reporter system of transcription, we identified more than 100 genes of V. cholerae induced upon exposure to the nematode Caenorhabditis elegans, which emerged recently as a valuable model for environmental predation during the aquatic lifestyle of V. cholerae. Besides others, we identified and validated the genes encoding the mannose-sensitive hemagglutinin (MSHA) type IV pilus to be significantly induced upon exposure to the nematode. Subsequent analyses demonstrated that the mannose-sensitive hemagglutinin is crucial for attachment of V. cholerae in the pharynx of the worm and initiation of colonization, which results in growth retardation and developmental delay of C. elegans. Thus, the surface adhesion factor MSHA could be linked to a fitness advantage of V. cholerae upon contact with bacterium-grazing nematodes. IMPORTANCE The waterborne diarrheal disease cholera is caused by the bacterium Vibrio cholerae. The facultative human pathogen persists as a natural inhabitant in the aquatic ecosystem between outbreaks. In contrast to the human host, V. cholerae requires a different set of genes to survive in this hostile environment. For example, predatory micrograzers are commonly found in the aquatic environment and use bacteria as a nutrient source, but knowledge of the interaction between bacterivorous grazers and V. cholerae is limited. In this study, we successfully adapted a genetic reporter technology and identified more than 100 genes activated by V. cholerae upon exposure to the bacterium-grazing nematode Caenorhabditis elegans. This screen provides a first glimpse into responses and adaptational strategies of the bacterial pathogen against such natural predators. Subsequent phenotypic characterization revealed the mannose-sensitive hemagglutinin to be crucial for colonization of the worm, which causes developmental delay and growth retardation.
format article
author Cornelia List
Andreas Grutsch
Claudia Radler
Fatih Cakar
Franz G. Zingl
Kristina Schild-Prüfert
Stefan Schild
author_facet Cornelia List
Andreas Grutsch
Claudia Radler
Fatih Cakar
Franz G. Zingl
Kristina Schild-Prüfert
Stefan Schild
author_sort Cornelia List
title Genes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization
title_short Genes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization
title_full Genes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization
title_fullStr Genes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization
title_full_unstemmed Genes Activated by <italic toggle="yes">Vibrio cholerae</italic> upon Exposure to <italic toggle="yes">Caenorhabditis elegans</italic> Reveal the Mannose-Sensitive Hemagglutinin To Be Essential for Colonization
title_sort genes activated by <italic toggle="yes">vibrio cholerae</italic> upon exposure to <italic toggle="yes">caenorhabditis elegans</italic> reveal the mannose-sensitive hemagglutinin to be essential for colonization
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/2c619c7c9bcf4073a2232b1926b0bbcf
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