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Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies

Colony formation is key to many ecological and biotechnological processes. In its early stages, colony formation involves the concourse of a number of physical and biological parameters for generation of a distinct 3D structure—the specific influence of which remains unclear. We focused on a thus fa...

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Autores principales: Kim, Juhyun, de Lorenzo, Víctor, Goñi‐Moreno, Ángel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10667634/
https://www.ncbi.nlm.nih.gov/pubmed/37231623
http://dx.doi.org/10.1111/1758-2229.13182
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author Kim, Juhyun
de Lorenzo, Víctor
Goñi‐Moreno, Ángel
author_facet Kim, Juhyun
de Lorenzo, Víctor
Goñi‐Moreno, Ángel
author_sort Kim, Juhyun
collection PubMed
description Colony formation is key to many ecological and biotechnological processes. In its early stages, colony formation involves the concourse of a number of physical and biological parameters for generation of a distinct 3D structure—the specific influence of which remains unclear. We focused on a thus far neglected aspect of the process, specifically the consequences of the differential pressure experienced by cells in the middle of a colony versus that endured by bacteria located in the growing periphery. This feature was characterized experimentally in the soil bacterium Pseudomonas putida. Using an agent‐based model we recreated the growth of microcolonies in a scenario in which pressure was the only parameter affecting proliferation of cells. Simulations exposed that, due to constant collisions with other growing bacteria, cells have virtually no free space to move sideways, thereby delaying growth and boosting chances of overlapping on top of each other. This scenario was tested experimentally on agar surfaces. Comparison between experiments and simulations suggested that the inside/outside differential pressure determines growth, both timewise and in terms of spatial directions, eventually moulding colony shape. We thus argue that—at least in the case studied—mere physical pressure of growing cells suffices to explain key dynamics of colony formation.
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spelling pubmed-106676342023-05-25 Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies Kim, Juhyun de Lorenzo, Víctor Goñi‐Moreno, Ángel Environ Microbiol Rep Brief Reports Colony formation is key to many ecological and biotechnological processes. In its early stages, colony formation involves the concourse of a number of physical and biological parameters for generation of a distinct 3D structure—the specific influence of which remains unclear. We focused on a thus far neglected aspect of the process, specifically the consequences of the differential pressure experienced by cells in the middle of a colony versus that endured by bacteria located in the growing periphery. This feature was characterized experimentally in the soil bacterium Pseudomonas putida. Using an agent‐based model we recreated the growth of microcolonies in a scenario in which pressure was the only parameter affecting proliferation of cells. Simulations exposed that, due to constant collisions with other growing bacteria, cells have virtually no free space to move sideways, thereby delaying growth and boosting chances of overlapping on top of each other. This scenario was tested experimentally on agar surfaces. Comparison between experiments and simulations suggested that the inside/outside differential pressure determines growth, both timewise and in terms of spatial directions, eventually moulding colony shape. We thus argue that—at least in the case studied—mere physical pressure of growing cells suffices to explain key dynamics of colony formation. John Wiley & Sons, Inc. 2023-05-25 /pmc/articles/PMC10667634/ /pubmed/37231623 http://dx.doi.org/10.1111/1758-2229.13182 Text en © 2023 The Authors. Environmental Microbiology Reports published by Applied Microbiology International and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Brief Reports
Kim, Juhyun
de Lorenzo, Víctor
Goñi‐Moreno, Ángel
Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies
title Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies
title_full Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies
title_fullStr Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies
title_full_unstemmed Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies
title_short Pressure‐dependent growth controls 3D architecture of Pseudomonas putida microcolonies
title_sort pressure‐dependent growth controls 3d architecture of pseudomonas putida microcolonies
topic Brief Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10667634/
https://www.ncbi.nlm.nih.gov/pubmed/37231623
http://dx.doi.org/10.1111/1758-2229.13182
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