Microbial Range Expansions on Liquid Substrates

Despite the importance of fluid flow for transporting and organizing populations, few laboratory systems exist to systematically investigate the impact of advection on their spatial evolutionary dynamics. To address this problem, we study the morphology and genetic spatial structure of microbial col...

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Autores principales:	Severine Atis, Bryan T. Weinstein, Andrew W. Murray, David R. Nelson
Formato:	article
Lenguaje:	EN
Publicado:	American Physical Society 2019
Materias:	Physics QC1-999
Acceso en línea:	https://doaj.org/article/980ce8b2de81442788746fc2be98fc30
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spelling	oai:doaj.org-article:980ce8b2de81442788746fc2be98fc302021-12-02T11:08:30ZMicrobial Range Expansions on Liquid Substrates10.1103/PhysRevX.9.0210582160-3308https://doaj.org/article/980ce8b2de81442788746fc2be98fc302019-06-01T00:00:00Zhttp://doi.org/10.1103/PhysRevX.9.021058http://doi.org/10.1103/PhysRevX.9.021058https://doaj.org/toc/2160-3308Despite the importance of fluid flow for transporting and organizing populations, few laboratory systems exist to systematically investigate the impact of advection on their spatial evolutionary dynamics. To address this problem, we study the morphology and genetic spatial structure of microbial colonies growing on the surface of a nutrient-laden fluid 10^{4} to 10^{5} times more viscous than water in Petri dishes; the extreme but finite viscosity inhibits undesired thermal convection and allows populations to effectively live at the air-liquid interface due to capillary forces. We discover that S. cerevisiae (baker’s yeast) growing on a viscous liquid behave like “active matter”: They metabolically generate fluid flows many times larger than their unperturbed colony expansion speed, and that flow, in turn, can dramatically impact their colony morphology and spatial population genetics. We show that yeast cells generate fluid flows by consuming surrounding nutrients and decreasing the local substrate density, leading to misaligned fluid pressure and density contours, which ultimately generates vorticity via a thresholdless baroclinic instability. Numerical simulations with experimentally measured parameters demonstrate that an intense vortex ring is produced below the colony’s edge. As the viscosity of the substrate is lowered and the self-induced flow intensifies, we observe three distinct morphologies: At the highest viscosity, cell proliferation and movement produces compact circular colonies with, however, a stretched regime of exponential expansion; intermediate viscosities give rise to compact colonies with “fingers” that are usually monoclonal and then break into smaller cell clusters; at the lowest viscosity, the expanding colony fractures into many genetically diverse, mutually repelling, islandlike fragments that can colonize an entire 94-mm-diameter Petri dish within 36 hours. We propose a simple phenomenological model that predicts the early colony dynamics. Our results provide rich opportunities to study the interplay between fluid flow and spatial population genetics for future investigations.Severine AtisBryan T. WeinsteinAndrew W. MurrayDavid R. NelsonAmerican Physical SocietyarticlePhysicsQC1-999ENPhysical Review X, Vol 9, Iss 2, p 021058 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Physics QC1-999
spellingShingle	Physics QC1-999 Severine Atis Bryan T. Weinstein Andrew W. Murray David R. Nelson Microbial Range Expansions on Liquid Substrates
description	Despite the importance of fluid flow for transporting and organizing populations, few laboratory systems exist to systematically investigate the impact of advection on their spatial evolutionary dynamics. To address this problem, we study the morphology and genetic spatial structure of microbial colonies growing on the surface of a nutrient-laden fluid 10^{4} to 10^{5} times more viscous than water in Petri dishes; the extreme but finite viscosity inhibits undesired thermal convection and allows populations to effectively live at the air-liquid interface due to capillary forces. We discover that S. cerevisiae (baker’s yeast) growing on a viscous liquid behave like “active matter”: They metabolically generate fluid flows many times larger than their unperturbed colony expansion speed, and that flow, in turn, can dramatically impact their colony morphology and spatial population genetics. We show that yeast cells generate fluid flows by consuming surrounding nutrients and decreasing the local substrate density, leading to misaligned fluid pressure and density contours, which ultimately generates vorticity via a thresholdless baroclinic instability. Numerical simulations with experimentally measured parameters demonstrate that an intense vortex ring is produced below the colony’s edge. As the viscosity of the substrate is lowered and the self-induced flow intensifies, we observe three distinct morphologies: At the highest viscosity, cell proliferation and movement produces compact circular colonies with, however, a stretched regime of exponential expansion; intermediate viscosities give rise to compact colonies with “fingers” that are usually monoclonal and then break into smaller cell clusters; at the lowest viscosity, the expanding colony fractures into many genetically diverse, mutually repelling, islandlike fragments that can colonize an entire 94-mm-diameter Petri dish within 36 hours. We propose a simple phenomenological model that predicts the early colony dynamics. Our results provide rich opportunities to study the interplay between fluid flow and spatial population genetics for future investigations.
format	article
author	Severine Atis Bryan T. Weinstein Andrew W. Murray David R. Nelson
author_facet	Severine Atis Bryan T. Weinstein Andrew W. Murray David R. Nelson
author_sort	Severine Atis
title	Microbial Range Expansions on Liquid Substrates
title_short	Microbial Range Expansions on Liquid Substrates
title_full	Microbial Range Expansions on Liquid Substrates
title_fullStr	Microbial Range Expansions on Liquid Substrates
title_full_unstemmed	Microbial Range Expansions on Liquid Substrates
title_sort	microbial range expansions on liquid substrates
publisher	American Physical Society
publishDate	2019
url	https://doaj.org/article/980ce8b2de81442788746fc2be98fc30
work_keys_str_mv	AT severineatis microbialrangeexpansionsonliquidsubstrates AT bryantweinstein microbialrangeexpansionsonliquidsubstrates AT andrewwmurray microbialrangeexpansionsonliquidsubstrates AT davidrnelson microbialrangeexpansionsonliquidsubstrates
_version_	1718396233258631168

Microbial Range Expansions on Liquid Substrates

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