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Social motility of biofilm-like microcolonies in a gliding bacterium

Bacterial biofilms are aggregates of surface-associated cells embedded in an extracellular polysaccharide (EPS) matrix, and are typically stationary. Studies of bacterial collective movement have largely focused on swarming motility mediated by flagella or pili, in the absence of a biofilm. Here, we...

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Autores principales: Li, Chao, Hurley, Amanda, Hu, Wei, Warrick, Jay W., Lozano, Gabriel L., Ayuso, Jose M., Pan, Wenxiao, Handelsman, Jo, Beebe, David J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481357/
https://www.ncbi.nlm.nih.gov/pubmed/34588437
http://dx.doi.org/10.1038/s41467-021-25408-7
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author Li, Chao
Hurley, Amanda
Hu, Wei
Warrick, Jay W.
Lozano, Gabriel L.
Ayuso, Jose M.
Pan, Wenxiao
Handelsman, Jo
Beebe, David J.
author_facet Li, Chao
Hurley, Amanda
Hu, Wei
Warrick, Jay W.
Lozano, Gabriel L.
Ayuso, Jose M.
Pan, Wenxiao
Handelsman, Jo
Beebe, David J.
author_sort Li, Chao
collection PubMed
description Bacterial biofilms are aggregates of surface-associated cells embedded in an extracellular polysaccharide (EPS) matrix, and are typically stationary. Studies of bacterial collective movement have largely focused on swarming motility mediated by flagella or pili, in the absence of a biofilm. Here, we describe a unique mode of collective movement by a self-propelled, surface-associated biofilm-like multicellular structure. Flavobacterium johnsoniae cells, which move by gliding motility, self-assemble into spherical microcolonies with EPS cores when observed by an under-oil open microfluidic system. Small microcolonies merge, creating larger ones. Microscopic analysis and computer simulation indicate that microcolonies move by cells at the base of the structure, attached to the surface by one pole of the cell. Biochemical and mutant analyses show that an active process drives microcolony self-assembly and motility, which depend on the bacterial gliding apparatus. We hypothesize that this mode of collective bacterial movement on solid surfaces may play potential roles in biofilm dynamics, bacterial cargo transport, or microbial adaptation. However, whether this collective motility occurs on plant roots or soil particles, the native environment for F. johnsoniae, is unknown.
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spelling pubmed-84813572021-10-22 Social motility of biofilm-like microcolonies in a gliding bacterium Li, Chao Hurley, Amanda Hu, Wei Warrick, Jay W. Lozano, Gabriel L. Ayuso, Jose M. Pan, Wenxiao Handelsman, Jo Beebe, David J. Nat Commun Article Bacterial biofilms are aggregates of surface-associated cells embedded in an extracellular polysaccharide (EPS) matrix, and are typically stationary. Studies of bacterial collective movement have largely focused on swarming motility mediated by flagella or pili, in the absence of a biofilm. Here, we describe a unique mode of collective movement by a self-propelled, surface-associated biofilm-like multicellular structure. Flavobacterium johnsoniae cells, which move by gliding motility, self-assemble into spherical microcolonies with EPS cores when observed by an under-oil open microfluidic system. Small microcolonies merge, creating larger ones. Microscopic analysis and computer simulation indicate that microcolonies move by cells at the base of the structure, attached to the surface by one pole of the cell. Biochemical and mutant analyses show that an active process drives microcolony self-assembly and motility, which depend on the bacterial gliding apparatus. We hypothesize that this mode of collective bacterial movement on solid surfaces may play potential roles in biofilm dynamics, bacterial cargo transport, or microbial adaptation. However, whether this collective motility occurs on plant roots or soil particles, the native environment for F. johnsoniae, is unknown. Nature Publishing Group UK 2021-09-29 /pmc/articles/PMC8481357/ /pubmed/34588437 http://dx.doi.org/10.1038/s41467-021-25408-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Li, Chao
Hurley, Amanda
Hu, Wei
Warrick, Jay W.
Lozano, Gabriel L.
Ayuso, Jose M.
Pan, Wenxiao
Handelsman, Jo
Beebe, David J.
Social motility of biofilm-like microcolonies in a gliding bacterium
title Social motility of biofilm-like microcolonies in a gliding bacterium
title_full Social motility of biofilm-like microcolonies in a gliding bacterium
title_fullStr Social motility of biofilm-like microcolonies in a gliding bacterium
title_full_unstemmed Social motility of biofilm-like microcolonies in a gliding bacterium
title_short Social motility of biofilm-like microcolonies in a gliding bacterium
title_sort social motility of biofilm-like microcolonies in a gliding bacterium
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8481357/
https://www.ncbi.nlm.nih.gov/pubmed/34588437
http://dx.doi.org/10.1038/s41467-021-25408-7
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