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Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae

Biofilm formation is generally recognized as a bacterial defense mechanism against environmental threats, including antibiotics, bacteriophages, and leukocytes of the human immune system. Here, we show that for the human pathogen Vibrio cholerae, biofilm formation is not only a protective trait but...

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Autores principales: Vidakovic, Lucia, Mikhaleva, Sofya, Jeckel, Hannah, Nisnevich, Valerya, Strenger, Kerstin, Neuhaus, Konstantin, Raveendran, Keerthana, Ben-Moshe, Noa Bossel, Aznaourova, Marina, Nosho, Kazuki, Drescher, Antje, Schmeck, Bernd, Schulte, Leon N., Persat, Alexandre, Avraham, Roi, Drescher, Knut
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10256282/
https://www.ncbi.nlm.nih.gov/pubmed/37295405
http://dx.doi.org/10.1016/j.cell.2023.05.008
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author Vidakovic, Lucia
Mikhaleva, Sofya
Jeckel, Hannah
Nisnevich, Valerya
Strenger, Kerstin
Neuhaus, Konstantin
Raveendran, Keerthana
Ben-Moshe, Noa Bossel
Aznaourova, Marina
Nosho, Kazuki
Drescher, Antje
Schmeck, Bernd
Schulte, Leon N.
Persat, Alexandre
Avraham, Roi
Drescher, Knut
author_facet Vidakovic, Lucia
Mikhaleva, Sofya
Jeckel, Hannah
Nisnevich, Valerya
Strenger, Kerstin
Neuhaus, Konstantin
Raveendran, Keerthana
Ben-Moshe, Noa Bossel
Aznaourova, Marina
Nosho, Kazuki
Drescher, Antje
Schmeck, Bernd
Schulte, Leon N.
Persat, Alexandre
Avraham, Roi
Drescher, Knut
author_sort Vidakovic, Lucia
collection PubMed
description Biofilm formation is generally recognized as a bacterial defense mechanism against environmental threats, including antibiotics, bacteriophages, and leukocytes of the human immune system. Here, we show that for the human pathogen Vibrio cholerae, biofilm formation is not only a protective trait but also an aggressive trait to collectively predate different immune cells. We find that V. cholerae forms biofilms on the eukaryotic cell surface using an extracellular matrix comprising primarily mannose-sensitive hemagglutinin pili, toxin-coregulated pili, and the secreted colonization factor TcpF, which differs from the matrix composition of biofilms on other surfaces. These biofilms encase immune cells and establish a high local concentration of a secreted hemolysin to kill the immune cells before the biofilms disperse in a c-di-GMP-dependent manner. Together, these results uncover how bacteria employ biofilm formation as a multicellular strategy to invert the typical relationship between human immune cells as the hunters and bacteria as the hunted.
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spelling pubmed-102562822023-06-10 Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae Vidakovic, Lucia Mikhaleva, Sofya Jeckel, Hannah Nisnevich, Valerya Strenger, Kerstin Neuhaus, Konstantin Raveendran, Keerthana Ben-Moshe, Noa Bossel Aznaourova, Marina Nosho, Kazuki Drescher, Antje Schmeck, Bernd Schulte, Leon N. Persat, Alexandre Avraham, Roi Drescher, Knut Cell Article Biofilm formation is generally recognized as a bacterial defense mechanism against environmental threats, including antibiotics, bacteriophages, and leukocytes of the human immune system. Here, we show that for the human pathogen Vibrio cholerae, biofilm formation is not only a protective trait but also an aggressive trait to collectively predate different immune cells. We find that V. cholerae forms biofilms on the eukaryotic cell surface using an extracellular matrix comprising primarily mannose-sensitive hemagglutinin pili, toxin-coregulated pili, and the secreted colonization factor TcpF, which differs from the matrix composition of biofilms on other surfaces. These biofilms encase immune cells and establish a high local concentration of a secreted hemolysin to kill the immune cells before the biofilms disperse in a c-di-GMP-dependent manner. Together, these results uncover how bacteria employ biofilm formation as a multicellular strategy to invert the typical relationship between human immune cells as the hunters and bacteria as the hunted. Cell Press 2023-06-08 /pmc/articles/PMC10256282/ /pubmed/37295405 http://dx.doi.org/10.1016/j.cell.2023.05.008 Text en © 2023 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Vidakovic, Lucia
Mikhaleva, Sofya
Jeckel, Hannah
Nisnevich, Valerya
Strenger, Kerstin
Neuhaus, Konstantin
Raveendran, Keerthana
Ben-Moshe, Noa Bossel
Aznaourova, Marina
Nosho, Kazuki
Drescher, Antje
Schmeck, Bernd
Schulte, Leon N.
Persat, Alexandre
Avraham, Roi
Drescher, Knut
Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae
title Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae
title_full Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae
title_fullStr Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae
title_full_unstemmed Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae
title_short Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae
title_sort biofilm formation on human immune cells is a multicellular predation strategy of vibrio cholerae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10256282/
https://www.ncbi.nlm.nih.gov/pubmed/37295405
http://dx.doi.org/10.1016/j.cell.2023.05.008
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