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Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics

Species utilizing the same resources often fail to coexist for extended periods of time. Such competitive exclusion mechanisms potentially underly microbiome dynamics, causing breakdowns of communities composed of species with similar genetic backgrounds of resource utilization. Although genes respo...

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Autores principales: Fujita, Hiroaki, Ushio, Masayuki, Suzuki, Kenta, Abe, Masato S., Yamamichi, Masato, Okazaki, Yusuke, Canarini, Alberto, Hayashi, Ibuki, Fukushima, Keitaro, Fukuda, Shinji, Kiers, E. Toby, Toju, Hirokazu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10684785/
https://www.ncbi.nlm.nih.gov/pubmed/38033594
http://dx.doi.org/10.3389/fmicb.2023.1261137
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author Fujita, Hiroaki
Ushio, Masayuki
Suzuki, Kenta
Abe, Masato S.
Yamamichi, Masato
Okazaki, Yusuke
Canarini, Alberto
Hayashi, Ibuki
Fukushima, Keitaro
Fukuda, Shinji
Kiers, E. Toby
Toju, Hirokazu
author_facet Fujita, Hiroaki
Ushio, Masayuki
Suzuki, Kenta
Abe, Masato S.
Yamamichi, Masato
Okazaki, Yusuke
Canarini, Alberto
Hayashi, Ibuki
Fukushima, Keitaro
Fukuda, Shinji
Kiers, E. Toby
Toju, Hirokazu
author_sort Fujita, Hiroaki
collection PubMed
description Species utilizing the same resources often fail to coexist for extended periods of time. Such competitive exclusion mechanisms potentially underly microbiome dynamics, causing breakdowns of communities composed of species with similar genetic backgrounds of resource utilization. Although genes responsible for competitive exclusion among a small number of species have been investigated in pioneering studies, it remains a major challenge to integrate genomics and ecology for understanding stable coexistence in species-rich communities. Here, we examine whether community-scale analyses of functional gene redundancy can provide a useful platform for interpreting and predicting collapse of bacterial communities. Through 110-day time-series of experimental microbiome dynamics, we analyzed the metagenome-assembled genomes of co-occurring bacterial species. We then inferred ecological niche space based on the multivariate analysis of the genome compositions. The analysis allowed us to evaluate potential shifts in the level of niche overlap between species through time. We hypothesized that community-scale pressure of competitive exclusion could be evaluated by quantifying overlap of genetically determined resource-use profiles (metabolic pathway profiles) among coexisting species. We found that the degree of community compositional changes observed in the experimental microbiome was correlated with the magnitude of gene-repertoire overlaps among bacterial species, although the causation between the two variables deserves future extensive research. The metagenome-based analysis of genetic potential for competitive exclusion will help us forecast major events in microbiome dynamics such as sudden community collapse (i.e., dysbiosis).
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spelling pubmed-106847852023-11-30 Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics Fujita, Hiroaki Ushio, Masayuki Suzuki, Kenta Abe, Masato S. Yamamichi, Masato Okazaki, Yusuke Canarini, Alberto Hayashi, Ibuki Fukushima, Keitaro Fukuda, Shinji Kiers, E. Toby Toju, Hirokazu Front Microbiol Microbiology Species utilizing the same resources often fail to coexist for extended periods of time. Such competitive exclusion mechanisms potentially underly microbiome dynamics, causing breakdowns of communities composed of species with similar genetic backgrounds of resource utilization. Although genes responsible for competitive exclusion among a small number of species have been investigated in pioneering studies, it remains a major challenge to integrate genomics and ecology for understanding stable coexistence in species-rich communities. Here, we examine whether community-scale analyses of functional gene redundancy can provide a useful platform for interpreting and predicting collapse of bacterial communities. Through 110-day time-series of experimental microbiome dynamics, we analyzed the metagenome-assembled genomes of co-occurring bacterial species. We then inferred ecological niche space based on the multivariate analysis of the genome compositions. The analysis allowed us to evaluate potential shifts in the level of niche overlap between species through time. We hypothesized that community-scale pressure of competitive exclusion could be evaluated by quantifying overlap of genetically determined resource-use profiles (metabolic pathway profiles) among coexisting species. We found that the degree of community compositional changes observed in the experimental microbiome was correlated with the magnitude of gene-repertoire overlaps among bacterial species, although the causation between the two variables deserves future extensive research. The metagenome-based analysis of genetic potential for competitive exclusion will help us forecast major events in microbiome dynamics such as sudden community collapse (i.e., dysbiosis). Frontiers Media S.A. 2023-11-15 /pmc/articles/PMC10684785/ /pubmed/38033594 http://dx.doi.org/10.3389/fmicb.2023.1261137 Text en Copyright © 2023 Fujita, Ushio, Suzuki, Abe, Yamamichi, Okazaki, Canarini, Hayashi, Fukushima, Fukuda, Kiers and Toju. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Fujita, Hiroaki
Ushio, Masayuki
Suzuki, Kenta
Abe, Masato S.
Yamamichi, Masato
Okazaki, Yusuke
Canarini, Alberto
Hayashi, Ibuki
Fukushima, Keitaro
Fukuda, Shinji
Kiers, E. Toby
Toju, Hirokazu
Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics
title Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics
title_full Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics
title_fullStr Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics
title_full_unstemmed Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics
title_short Metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics
title_sort metagenomic analysis of ecological niche overlap and community collapse in microbiome dynamics
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10684785/
https://www.ncbi.nlm.nih.gov/pubmed/38033594
http://dx.doi.org/10.3389/fmicb.2023.1261137
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