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Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut
The vertebrate intestine is home to microbial ecosystems that play key roles in host development and health. Little is known about the spatial and temporal dynamics of these microbial communities, limiting our understanding of fundamental properties, such as their mechanisms of growth, propagation,...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society of Microbiology
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4271548/ https://www.ncbi.nlm.nih.gov/pubmed/25516613 http://dx.doi.org/10.1128/mBio.01751-14 |
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author | Jemielita, Matthew Taormina, Michael J. Burns, Adam R. Hampton, Jennifer S. Rolig, Annah S. Guillemin, Karen Parthasarathy, Raghuveer |
author_facet | Jemielita, Matthew Taormina, Michael J. Burns, Adam R. Hampton, Jennifer S. Rolig, Annah S. Guillemin, Karen Parthasarathy, Raghuveer |
author_sort | Jemielita, Matthew |
collection | PubMed |
description | The vertebrate intestine is home to microbial ecosystems that play key roles in host development and health. Little is known about the spatial and temporal dynamics of these microbial communities, limiting our understanding of fundamental properties, such as their mechanisms of growth, propagation, and persistence. To address this, we inoculated initially germ-free zebrafish larvae with fluorescently labeled strains of an Aeromonas species, representing an abundant genus in the zebrafish gut. Using light sheet fluorescence microscopy to obtain three-dimensional images spanning the gut, we quantified the entire bacterial load, as founding populations grew from tens to tens of thousands of cells over several hours. The data yield the first ever measurements of the growth kinetics of a microbial species inside a live vertebrate intestine and show dynamics that robustly fit a logistic growth model. Intriguingly, bacteria were nonuniformly distributed throughout the gut, and bacterial aggregates showed considerably higher growth rates than did discrete individuals. The form of aggregate growth indicates intrinsically higher division rates for clustered bacteria, rather than surface-mediated agglomeration onto clusters. Thus, the spatial organization of gut bacteria both relative to the host and to each other impacts overall growth kinetics, suggesting that spatial characterizations will be an important input to predictive models of host-associated microbial community assembly. |
format | Online Article Text |
id | pubmed-4271548 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | American Society of Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-42715482014-12-31 Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut Jemielita, Matthew Taormina, Michael J. Burns, Adam R. Hampton, Jennifer S. Rolig, Annah S. Guillemin, Karen Parthasarathy, Raghuveer mBio Research Article The vertebrate intestine is home to microbial ecosystems that play key roles in host development and health. Little is known about the spatial and temporal dynamics of these microbial communities, limiting our understanding of fundamental properties, such as their mechanisms of growth, propagation, and persistence. To address this, we inoculated initially germ-free zebrafish larvae with fluorescently labeled strains of an Aeromonas species, representing an abundant genus in the zebrafish gut. Using light sheet fluorescence microscopy to obtain three-dimensional images spanning the gut, we quantified the entire bacterial load, as founding populations grew from tens to tens of thousands of cells over several hours. The data yield the first ever measurements of the growth kinetics of a microbial species inside a live vertebrate intestine and show dynamics that robustly fit a logistic growth model. Intriguingly, bacteria were nonuniformly distributed throughout the gut, and bacterial aggregates showed considerably higher growth rates than did discrete individuals. The form of aggregate growth indicates intrinsically higher division rates for clustered bacteria, rather than surface-mediated agglomeration onto clusters. Thus, the spatial organization of gut bacteria both relative to the host and to each other impacts overall growth kinetics, suggesting that spatial characterizations will be an important input to predictive models of host-associated microbial community assembly. American Society of Microbiology 2014-12-16 /pmc/articles/PMC4271548/ /pubmed/25516613 http://dx.doi.org/10.1128/mBio.01751-14 Text en Copyright © 2014 Jemielita et al. http://creativecommons.org/licenses/by-nc-sa/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license (http://creativecommons.org/licenses/by-nc-sa/3.0/) , which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Jemielita, Matthew Taormina, Michael J. Burns, Adam R. Hampton, Jennifer S. Rolig, Annah S. Guillemin, Karen Parthasarathy, Raghuveer Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut |
title | Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut |
title_full | Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut |
title_fullStr | Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut |
title_full_unstemmed | Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut |
title_short | Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut |
title_sort | spatial and temporal features of the growth of a bacterial species colonizing the zebrafish gut |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4271548/ https://www.ncbi.nlm.nih.gov/pubmed/25516613 http://dx.doi.org/10.1128/mBio.01751-14 |
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