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The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations

BACKGROUND: Bacterial habitats, such as soil and the gut, are structured at the micrometer scale. Important aspects of microbial life in such spatial ecosystems are migration and colonization. Here we explore the colonization of a structured ecosystem by two neutrally labeled strains of Escherichia...

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Autores principales: van Vliet, Simon, Hol, Felix JH, Weenink, Tim, Galajda, Peter, Keymer, Juan E
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4032360/
https://www.ncbi.nlm.nih.gov/pubmed/24884963
http://dx.doi.org/10.1186/1471-2180-14-116
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author van Vliet, Simon
Hol, Felix JH
Weenink, Tim
Galajda, Peter
Keymer, Juan E
author_facet van Vliet, Simon
Hol, Felix JH
Weenink, Tim
Galajda, Peter
Keymer, Juan E
author_sort van Vliet, Simon
collection PubMed
description BACKGROUND: Bacterial habitats, such as soil and the gut, are structured at the micrometer scale. Important aspects of microbial life in such spatial ecosystems are migration and colonization. Here we explore the colonization of a structured ecosystem by two neutrally labeled strains of Escherichia coli. Using time-lapse microscopy we studied the colonization of one-dimensional arrays of habitat patches linked by connectors, which were invaded by the two E. coli strains from opposite sides. RESULTS: The two strains colonize a habitat from opposite sides by a series of traveling waves followed by an expansion front. When population waves collide, they branch into a continuing traveling wave, a reflected wave and a stationary population. When the two strains invade the landscape from opposite sides, they remain segregated in space and often one population will displace the other from most of the habitat. However, when the strains are co-cultured before entering the habitats, they colonize the habitat together and do not separate spatially. Using physically separated, but diffusionally coupled, habitats we show that colonization waves and expansion fronts interact trough diffusible molecules, and not by direct competition for space. Furthermore, we found that colonization outcome is influenced by a culture’s history, as the culture with the longest doubling time in bulk conditions tends to take over the largest fraction of the habitat. Finally, we observed that population distributions in parallel habitats located on the same device and inoculated with cells from the same overnight culture are significantly more similar to each other than to patterns in identical habitats located on different devices inoculated with cells from different overnight cultures, even tough all cultures were started from the same −80°C frozen stock. CONCLUSIONS: We found that the colonization of spatially structure habitats by two interacting populations can lead to the formation of complex, but reproducible, spatiotemporal patterns. Furthermore, we showed that chemical interactions between two populations cause them to remain spatially segregated while they compete for habitat space. Finally, we observed that growth properties in bulk conditions correlate with the outcome of habitat colonization. Together, our data show the crucial roles of chemical interactions between populations and a culture’s history in determining the outcome of habitat colonization.
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spelling pubmed-40323602014-06-10 The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations van Vliet, Simon Hol, Felix JH Weenink, Tim Galajda, Peter Keymer, Juan E BMC Microbiol Research Article BACKGROUND: Bacterial habitats, such as soil and the gut, are structured at the micrometer scale. Important aspects of microbial life in such spatial ecosystems are migration and colonization. Here we explore the colonization of a structured ecosystem by two neutrally labeled strains of Escherichia coli. Using time-lapse microscopy we studied the colonization of one-dimensional arrays of habitat patches linked by connectors, which were invaded by the two E. coli strains from opposite sides. RESULTS: The two strains colonize a habitat from opposite sides by a series of traveling waves followed by an expansion front. When population waves collide, they branch into a continuing traveling wave, a reflected wave and a stationary population. When the two strains invade the landscape from opposite sides, they remain segregated in space and often one population will displace the other from most of the habitat. However, when the strains are co-cultured before entering the habitats, they colonize the habitat together and do not separate spatially. Using physically separated, but diffusionally coupled, habitats we show that colonization waves and expansion fronts interact trough diffusible molecules, and not by direct competition for space. Furthermore, we found that colonization outcome is influenced by a culture’s history, as the culture with the longest doubling time in bulk conditions tends to take over the largest fraction of the habitat. Finally, we observed that population distributions in parallel habitats located on the same device and inoculated with cells from the same overnight culture are significantly more similar to each other than to patterns in identical habitats located on different devices inoculated with cells from different overnight cultures, even tough all cultures were started from the same −80°C frozen stock. CONCLUSIONS: We found that the colonization of spatially structure habitats by two interacting populations can lead to the formation of complex, but reproducible, spatiotemporal patterns. Furthermore, we showed that chemical interactions between two populations cause them to remain spatially segregated while they compete for habitat space. Finally, we observed that growth properties in bulk conditions correlate with the outcome of habitat colonization. Together, our data show the crucial roles of chemical interactions between populations and a culture’s history in determining the outcome of habitat colonization. BioMed Central 2014-05-07 /pmc/articles/PMC4032360/ /pubmed/24884963 http://dx.doi.org/10.1186/1471-2180-14-116 Text en Copyright © 2014 van Vliet et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
van Vliet, Simon
Hol, Felix JH
Weenink, Tim
Galajda, Peter
Keymer, Juan E
The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations
title The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations
title_full The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations
title_fullStr The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations
title_full_unstemmed The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations
title_short The effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations
title_sort effects of chemical interactions and culture history on the colonization of structured habitats by competing bacterial populations
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4032360/
https://www.ncbi.nlm.nih.gov/pubmed/24884963
http://dx.doi.org/10.1186/1471-2180-14-116
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