Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data

ABSTRACT A priority in gut microbiome research is to develop methods to investigate ecological processes shaping microbial populations in the host from readily accessible data, such as fecal samples. Here, we demonstrate that these processes can be inferred from the proportion of ingested microorgan...

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Autores principales:	Hidetoshi Inamine, Stephen P. Ellner, Peter D. Newell, Yuan Luo, Nicolas Buchon, Angela E. Douglas
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Acetobacter tropicalis Drosophila melanogaster gut microbiota microbial ecology population dynamics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a6a630256e9a4d09b016a3f7461e246b
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spelling	oai:doaj.org-article:a6a630256e9a4d09b016a3f7461e246b2021-11-15T15:53:25ZSpatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data10.1128/mBio.01453-172150-7511https://doaj.org/article/a6a630256e9a4d09b016a3f7461e246b2018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01453-17https://doaj.org/toc/2150-7511ABSTRACT A priority in gut microbiome research is to develop methods to investigate ecological processes shaping microbial populations in the host from readily accessible data, such as fecal samples. Here, we demonstrate that these processes can be inferred from the proportion of ingested microorganisms that is egested and their egestion time distribution, by using general mathematical models that link within-host processes to statistics from fecal time series. We apply this framework to Drosophila melanogaster and its gut bacterium Acetobacter tropicalis. Specifically, we investigate changes in their interactions following ingestion of a food bolus containing bacteria in a set of treatments varying the following key parameters: the density of exogenous bacteria ingested by the flies (low/high) and the association status of the host (axenic or monoassociated with A. tropicalis). At 5 h post-ingestion, ~35% of the intact bacterial cells have transited through the gut with the food bolus and ~10% are retained in a viable and culturable state, leaving ~55% that have likely been lysed in the gut. Our models imply that lysis and retention occur over a short spatial range within the gut when the bacteria are ingested from a low density, but more broadly in the host gut when ingested from a high density, by both gnotobiotic and axenic hosts. Our study illustrates how time series data complement the analysis of static abundance patterns to infer ecological processes as bacteria traverse the host. Our approach can be extended to investigate how different bacterial species interact within the host to understand the processes shaping microbial community assembly. IMPORTANCE A major challenge to our understanding of the gut microbiome in animals is that it is profoundly difficult to investigate the fate of ingested microbial cells as they travel through the gut. Here, we created mathematical tools to analyze microbial dynamics in the gut from the temporal pattern of their abundance in fecal samples, i.e., without direct observation of the dynamics, and validated them with Drosophila fruit flies. Our analyses revealed that over 5 h after ingestion, most bacteria have likely died in the host or have been egested as intact cells, while some living cells have been retained in the host. Bacterial lysis or retention occurred across a larger area of the gut when flies ingest bacteria from high densities than when flies ingest bacteria from low densities. Our mathematical tools can be applied to other systems, including the dynamics of gut microbial populations and communities in humans.Hidetoshi InamineStephen P. EllnerPeter D. NewellYuan LuoNicolas BuchonAngela E. DouglasAmerican Society for MicrobiologyarticleAcetobacter tropicalisDrosophila melanogastergut microbiotamicrobial ecologypopulation dynamicsMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Acetobacter tropicalis Drosophila melanogaster gut microbiota microbial ecology population dynamics Microbiology QR1-502
spellingShingle	Acetobacter tropicalis Drosophila melanogaster gut microbiota microbial ecology population dynamics Microbiology QR1-502 Hidetoshi Inamine Stephen P. Ellner Peter D. Newell Yuan Luo Nicolas Buchon Angela E. Douglas Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data
description	ABSTRACT A priority in gut microbiome research is to develop methods to investigate ecological processes shaping microbial populations in the host from readily accessible data, such as fecal samples. Here, we demonstrate that these processes can be inferred from the proportion of ingested microorganisms that is egested and their egestion time distribution, by using general mathematical models that link within-host processes to statistics from fecal time series. We apply this framework to Drosophila melanogaster and its gut bacterium Acetobacter tropicalis. Specifically, we investigate changes in their interactions following ingestion of a food bolus containing bacteria in a set of treatments varying the following key parameters: the density of exogenous bacteria ingested by the flies (low/high) and the association status of the host (axenic or monoassociated with A. tropicalis). At 5 h post-ingestion, ~35% of the intact bacterial cells have transited through the gut with the food bolus and ~10% are retained in a viable and culturable state, leaving ~55% that have likely been lysed in the gut. Our models imply that lysis and retention occur over a short spatial range within the gut when the bacteria are ingested from a low density, but more broadly in the host gut when ingested from a high density, by both gnotobiotic and axenic hosts. Our study illustrates how time series data complement the analysis of static abundance patterns to infer ecological processes as bacteria traverse the host. Our approach can be extended to investigate how different bacterial species interact within the host to understand the processes shaping microbial community assembly. IMPORTANCE A major challenge to our understanding of the gut microbiome in animals is that it is profoundly difficult to investigate the fate of ingested microbial cells as they travel through the gut. Here, we created mathematical tools to analyze microbial dynamics in the gut from the temporal pattern of their abundance in fecal samples, i.e., without direct observation of the dynamics, and validated them with Drosophila fruit flies. Our analyses revealed that over 5 h after ingestion, most bacteria have likely died in the host or have been egested as intact cells, while some living cells have been retained in the host. Bacterial lysis or retention occurred across a larger area of the gut when flies ingest bacteria from high densities than when flies ingest bacteria from low densities. Our mathematical tools can be applied to other systems, including the dynamics of gut microbial populations and communities in humans.
format	article
author	Hidetoshi Inamine Stephen P. Ellner Peter D. Newell Yuan Luo Nicolas Buchon Angela E. Douglas
author_facet	Hidetoshi Inamine Stephen P. Ellner Peter D. Newell Yuan Luo Nicolas Buchon Angela E. Douglas
author_sort	Hidetoshi Inamine
title	Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data
title_short	Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data
title_full	Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data
title_fullStr	Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data
title_full_unstemmed	Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data
title_sort	spatiotemporally heterogeneous population dynamics of gut bacteria inferred from fecal time series data
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/a6a630256e9a4d09b016a3f7461e246b
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Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data

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