Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut

ABSTRACT 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, prop...

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Autores principales:	Matthew Jemielita, Michael J. Taormina, Adam R. Burns, Jennifer S. Hampton, Annah S. Rolig, Karen Guillemin, Raghuveer Parthasarathy
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b8905efcac6b412cbd8e48a8e58cfb79
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spelling	oai:doaj.org-article:b8905efcac6b412cbd8e48a8e58cfb792021-11-15T15:47:04ZSpatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut10.1128/mBio.01751-142150-7511https://doaj.org/article/b8905efcac6b412cbd8e48a8e58cfb792014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01751-14https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Our intestines are home to vast numbers of microbes that influence many aspects of health and disease. Though we now know a great deal about the constituents of the gut microbiota, we understand very little about their spatial structure and temporal dynamics in humans or in any animal: how microbial populations establish themselves, grow, fluctuate, and persist. To address this, we made use of a model organism, the zebrafish, and a new optical imaging technique, light sheet fluorescence microscopy, to visualize for the first time the colonization of a live, vertebrate gut by specific bacteria with sufficient resolution to quantify the population over a range from a few individuals to tens of thousands of bacterial cells. Our results provide unprecedented measures of bacterial growth kinetics and also show the influence of spatial structure on bacterial populations, which can be revealed only by direct imaging.Matthew JemielitaMichael J. TaorminaAdam R. BurnsJennifer S. HamptonAnnah S. RoligKaren GuilleminRaghuveer ParthasarathyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Matthew Jemielita Michael J. Taormina Adam R. Burns Jennifer S. Hampton Annah S. Rolig Karen Guillemin Raghuveer Parthasarathy Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut
description	ABSTRACT 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. IMPORTANCE Our intestines are home to vast numbers of microbes that influence many aspects of health and disease. Though we now know a great deal about the constituents of the gut microbiota, we understand very little about their spatial structure and temporal dynamics in humans or in any animal: how microbial populations establish themselves, grow, fluctuate, and persist. To address this, we made use of a model organism, the zebrafish, and a new optical imaging technique, light sheet fluorescence microscopy, to visualize for the first time the colonization of a live, vertebrate gut by specific bacteria with sufficient resolution to quantify the population over a range from a few individuals to tens of thousands of bacterial cells. Our results provide unprecedented measures of bacterial growth kinetics and also show the influence of spatial structure on bacterial populations, which can be revealed only by direct imaging.
format	article
author	Matthew Jemielita Michael J. Taormina Adam R. Burns Jennifer S. Hampton Annah S. Rolig Karen Guillemin Raghuveer Parthasarathy
author_facet	Matthew Jemielita Michael J. Taormina Adam R. Burns Jennifer S. Hampton Annah S. Rolig Karen Guillemin Raghuveer Parthasarathy
author_sort	Matthew Jemielita
title	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_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_sort	spatial and temporal features of the growth of a bacterial species colonizing the zebrafish gut
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/b8905efcac6b412cbd8e48a8e58cfb79
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Spatial and Temporal Features of the Growth of a Bacterial Species Colonizing the Zebrafish Gut

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