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

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...

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Main Authors: Hidetoshi Inamine, Stephen P. Ellner, Peter D. Newell, Yuan Luo, Nicolas Buchon, Angela E. Douglas, David A. Relman
Format: Article
Language:English
Published: American Society for Microbiology 2018-01-01
Series:mBio
Online Access:http://mbio.asm.org/cgi/content/full/9/1/e01453-17
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spelling doaj-bc9c9cfa724e4689989d04f5977d90a62021-07-02T09:22:45ZengAmerican Society for MicrobiologymBio2150-75112018-01-0191e01453-1710.1128/mBio.01453-17Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series DataHidetoshi InamineStephen P. EllnerPeter D. NewellYuan LuoNicolas BuchonAngela E. DouglasDavid A. RelmanA 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.http://mbio.asm.org/cgi/content/full/9/1/e01453-17
collection DOAJ
language English
format Article
sources DOAJ
author Hidetoshi Inamine
Stephen P. Ellner
Peter D. Newell
Yuan Luo
Nicolas Buchon
Angela E. Douglas
David A. Relman
spellingShingle Hidetoshi Inamine
Stephen P. Ellner
Peter D. Newell
Yuan Luo
Nicolas Buchon
Angela E. Douglas
David A. Relman
Spatiotemporally Heterogeneous Population Dynamics of Gut Bacteria Inferred from Fecal Time Series Data
mBio
author_facet Hidetoshi Inamine
Stephen P. Ellner
Peter D. Newell
Yuan Luo
Nicolas Buchon
Angela E. Douglas
David A. Relman
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
series mBio
issn 2150-7511
publishDate 2018-01-01
description 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.
url http://mbio.asm.org/cgi/content/full/9/1/e01453-17
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