Cargando…

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,...

Descripción completa

Detalles Bibliográficos
Autores principales: Jemielita, Matthew, Taormina, Michael J., Burns, Adam R., Hampton, Jennifer S., Rolig, Annah S., Guillemin, Karen, Parthasarathy, Raghuveer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society of Microbiology 2014
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
_version_ 1782349624690868224
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
work_keys_str_mv AT jemielitamatthew spatialandtemporalfeaturesofthegrowthofabacterialspeciescolonizingthezebrafishgut
AT taorminamichaelj spatialandtemporalfeaturesofthegrowthofabacterialspeciescolonizingthezebrafishgut
AT burnsadamr spatialandtemporalfeaturesofthegrowthofabacterialspeciescolonizingthezebrafishgut
AT hamptonjennifers spatialandtemporalfeaturesofthegrowthofabacterialspeciescolonizingthezebrafishgut
AT roligannahs spatialandtemporalfeaturesofthegrowthofabacterialspeciescolonizingthezebrafishgut
AT guilleminkaren spatialandtemporalfeaturesofthegrowthofabacterialspeciescolonizingthezebrafishgut
AT parthasarathyraghuveer spatialandtemporalfeaturesofthegrowthofabacterialspeciescolonizingthezebrafishgut