Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota

ABSTRACT The gastrointestinal (GI) microbiome is a densely populated ecosystem where dynamics are determined by interactions between microbial community members, as well as host factors. The spatial organization of this system is thought to be important in human health, yet this aspect of our reside...

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Autores principales:	Eric J. de Muinck, Knut E. A. Lundin, Pål Trosvik
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	16S rRNA gene microbiome biotic interactions intestine microbial ecology spatial structure Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/36c00a6e05034860807162dd9adc1d6e
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spelling	oai:doaj.org-article:36c00a6e05034860807162dd9adc1d6e2021-12-02T19:45:29ZLinking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota10.1128/mSystems.00086-172379-5077https://doaj.org/article/36c00a6e05034860807162dd9adc1d6e2017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00086-17https://doaj.org/toc/2379-5077ABSTRACT The gastrointestinal (GI) microbiome is a densely populated ecosystem where dynamics are determined by interactions between microbial community members, as well as host factors. The spatial organization of this system is thought to be important in human health, yet this aspect of our resident microbiome is still poorly understood. In this study, we report significant spatial structure of the GI microbiota, and we identify general categories of spatial patterning in the distribution of microbial taxa along a healthy human GI tract. We further estimate the biotic interaction structure in the GI microbiota, both through time series and cooccurrence modeling of microbial community data derived from a large number of sequentially collected fecal samples. Comparison of these two approaches showed that species pairs involved in significant negative interactions had strong positive contemporaneous correlations and vice versa, while for species pairs without significant interactions, contemporaneous correlations were distributed around zero. We observed similar patterns when comparing these models to the spatial correlations between taxa identified in the adherent microbiota. This suggests that colocalization of microbial taxon pairs, and thus the spatial organization of the GI microbiota, is driven, at least in part, by direct or indirect biotic interactions. Thus, our study can provide a basis for an ecological interpretation of the biogeography of the human gut. IMPORTANCE The human gut microbiome is the subject of intense study due to its importance in health and disease. The majority of these studies have been based on the analysis of feces. However, little is known about how the microbial composition in fecal samples relates to the spatial distribution of microbial taxa along the gastrointestinal tract. By characterizing the microbial content both in intestinal tissue samples and in fecal samples obtained daily, we provide a conceptual framework for how the spatial structure relates to biotic interactions on the community level. We further describe general categories of spatial distribution patterns and identify taxa conforming to these categories. To our knowledge, this is the first study combining spatial and temporal analyses of the human gut microbiome. This type of analysis can be used for identifying candidate probiotics and designing strategies for clinical intervention. Author Video: An author video summary of this article is available.Eric J. de MuinckKnut E. A. LundinPål TrosvikAmerican Society for Microbiologyarticle16S rRNA genemicrobiomebiotic interactionsintestinemicrobial ecologyspatial structureMicrobiologyQR1-502ENmSystems, Vol 2, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	16S rRNA gene microbiome biotic interactions intestine microbial ecology spatial structure Microbiology QR1-502
spellingShingle	16S rRNA gene microbiome biotic interactions intestine microbial ecology spatial structure Microbiology QR1-502 Eric J. de Muinck Knut E. A. Lundin Pål Trosvik Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota
description	ABSTRACT The gastrointestinal (GI) microbiome is a densely populated ecosystem where dynamics are determined by interactions between microbial community members, as well as host factors. The spatial organization of this system is thought to be important in human health, yet this aspect of our resident microbiome is still poorly understood. In this study, we report significant spatial structure of the GI microbiota, and we identify general categories of spatial patterning in the distribution of microbial taxa along a healthy human GI tract. We further estimate the biotic interaction structure in the GI microbiota, both through time series and cooccurrence modeling of microbial community data derived from a large number of sequentially collected fecal samples. Comparison of these two approaches showed that species pairs involved in significant negative interactions had strong positive contemporaneous correlations and vice versa, while for species pairs without significant interactions, contemporaneous correlations were distributed around zero. We observed similar patterns when comparing these models to the spatial correlations between taxa identified in the adherent microbiota. This suggests that colocalization of microbial taxon pairs, and thus the spatial organization of the GI microbiota, is driven, at least in part, by direct or indirect biotic interactions. Thus, our study can provide a basis for an ecological interpretation of the biogeography of the human gut. IMPORTANCE The human gut microbiome is the subject of intense study due to its importance in health and disease. The majority of these studies have been based on the analysis of feces. However, little is known about how the microbial composition in fecal samples relates to the spatial distribution of microbial taxa along the gastrointestinal tract. By characterizing the microbial content both in intestinal tissue samples and in fecal samples obtained daily, we provide a conceptual framework for how the spatial structure relates to biotic interactions on the community level. We further describe general categories of spatial distribution patterns and identify taxa conforming to these categories. To our knowledge, this is the first study combining spatial and temporal analyses of the human gut microbiome. This type of analysis can be used for identifying candidate probiotics and designing strategies for clinical intervention. Author Video: An author video summary of this article is available.
format	article
author	Eric J. de Muinck Knut E. A. Lundin Pål Trosvik
author_facet	Eric J. de Muinck Knut E. A. Lundin Pål Trosvik
author_sort	Eric J. de Muinck
title	Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota
title_short	Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota
title_full	Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota
title_fullStr	Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota
title_full_unstemmed	Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota
title_sort	linking spatial structure and community-level biotic interactions through cooccurrence and time series modeling of the human intestinal microbiota
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/36c00a6e05034860807162dd9adc1d6e
work_keys_str_mv	AT ericjdemuinck linkingspatialstructureandcommunitylevelbioticinteractionsthroughcooccurrenceandtimeseriesmodelingofthehumanintestinalmicrobiota AT knutealundin linkingspatialstructureandcommunitylevelbioticinteractionsthroughcooccurrenceandtimeseriesmodelingofthehumanintestinalmicrobiota AT paltrosvik linkingspatialstructureandcommunitylevelbioticinteractionsthroughcooccurrenceandtimeseriesmodelingofthehumanintestinalmicrobiota
_version_	1718376017976885248

Linking Spatial Structure and Community-Level Biotic Interactions through Cooccurrence and Time Series Modeling of the Human Intestinal Microbiota

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