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Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms
Collective behavior in spatially structured groups, or biofilms, is the norm among microbes in their natural environments. Though biofilm formation has been studied for decades, tracing the mechanistic and ecological links between individual cell morphologies and the emergent features of cell groups...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6628660/ https://www.ncbi.nlm.nih.gov/pubmed/31239347 http://dx.doi.org/10.1073/pnas.1819016116 |
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author | Wucher, Benjamin R. Bartlett, Thomas M. Hoyos, Mona Papenfort, Kai Persat, Alexandre Nadell, Carey D. |
author_facet | Wucher, Benjamin R. Bartlett, Thomas M. Hoyos, Mona Papenfort, Kai Persat, Alexandre Nadell, Carey D. |
author_sort | Wucher, Benjamin R. |
collection | PubMed |
description | Collective behavior in spatially structured groups, or biofilms, is the norm among microbes in their natural environments. Though biofilm formation has been studied for decades, tracing the mechanistic and ecological links between individual cell morphologies and the emergent features of cell groups is still in its infancy. Here we use single-cell–resolution confocal microscopy to explore biofilms of the human pathogen Vibrio cholerae in conditions mimicking its marine habitat. Prior reports have noted the occurrence of cellular filamentation in V. cholerae, with variable propensity to filament among both toxigenic and nontoxigenic strains. Using a filamenting strain of V. cholerae O139, we show that cells with this morphotype gain a profound competitive advantage in colonizing and spreading on particles of chitin, the material many marine Vibrio species depend on for growth in seawater. Furthermore, filamentous cells can produce biofilms that are independent of primary secreted components of the V. cholerae biofilm matrix; instead, filamentous biofilm architectural strength appears to derive at least in part from the entangled mesh of cells themselves. The advantage gained by filamentous cells in early chitin colonization and growth is countered in long-term competition experiments with matrix-secreting V. cholerae variants, whose densely packed biofilm structures displace competitors from surfaces. Overall, our results reveal an alternative mode of biofilm architecture that is dependent on filamentous cell morphology and advantageous in environments with rapid chitin particle turnover. This insight provides an environmentally relevant example of how cell morphology can impact bacterial fitness. |
format | Online Article Text |
id | pubmed-6628660 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-66286602019-07-22 Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms Wucher, Benjamin R. Bartlett, Thomas M. Hoyos, Mona Papenfort, Kai Persat, Alexandre Nadell, Carey D. Proc Natl Acad Sci U S A Biological Sciences Collective behavior in spatially structured groups, or biofilms, is the norm among microbes in their natural environments. Though biofilm formation has been studied for decades, tracing the mechanistic and ecological links between individual cell morphologies and the emergent features of cell groups is still in its infancy. Here we use single-cell–resolution confocal microscopy to explore biofilms of the human pathogen Vibrio cholerae in conditions mimicking its marine habitat. Prior reports have noted the occurrence of cellular filamentation in V. cholerae, with variable propensity to filament among both toxigenic and nontoxigenic strains. Using a filamenting strain of V. cholerae O139, we show that cells with this morphotype gain a profound competitive advantage in colonizing and spreading on particles of chitin, the material many marine Vibrio species depend on for growth in seawater. Furthermore, filamentous cells can produce biofilms that are independent of primary secreted components of the V. cholerae biofilm matrix; instead, filamentous biofilm architectural strength appears to derive at least in part from the entangled mesh of cells themselves. The advantage gained by filamentous cells in early chitin colonization and growth is countered in long-term competition experiments with matrix-secreting V. cholerae variants, whose densely packed biofilm structures displace competitors from surfaces. Overall, our results reveal an alternative mode of biofilm architecture that is dependent on filamentous cell morphology and advantageous in environments with rapid chitin particle turnover. This insight provides an environmentally relevant example of how cell morphology can impact bacterial fitness. National Academy of Sciences 2019-07-09 2019-06-25 /pmc/articles/PMC6628660/ /pubmed/31239347 http://dx.doi.org/10.1073/pnas.1819016116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Wucher, Benjamin R. Bartlett, Thomas M. Hoyos, Mona Papenfort, Kai Persat, Alexandre Nadell, Carey D. Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms |
title | Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms |
title_full | Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms |
title_fullStr | Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms |
title_full_unstemmed | Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms |
title_short | Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms |
title_sort | vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6628660/ https://www.ncbi.nlm.nih.gov/pubmed/31239347 http://dx.doi.org/10.1073/pnas.1819016116 |
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