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

Hiroaki Fujita*, Masayuki Ushio, Kenta Suzuki, Masato S. Abe, Masato Yamamichi, Yusuke Okazaki, Alberto Canarini, Ibuki Hayashi, Keitaro Fukushima, Shinji Fukuda, E. Toby Kiers, Hirokazu Toju*

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

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).

Original languageEnglish
Article number1261137
Pages (from-to)1-11
Number of pages11
JournalFrontiers in Microbiology
Volume14
Early online date15 Nov 2023
DOIs
Publication statusPublished - 2023

Bibliographical note

Publisher Copyright:
Copyright © 2023 Fujita, Ushio, Suzuki, Abe, Yamamichi, Okazaki, Canarini, Hayashi, Fukushima, Fukuda, Kiers and Toju.

Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was financially supported by JST PRESTO (JPMJPR16Q6), Human Frontier Science Program (RGP0029/2019), JSPS Grant-in-Aid for Scientific Research (20K20586), NEDO Moonshot Research and Development Program (JPNP18016), JST FOREST (JPMJFR2048) to HT, JSPS Grant-in-Aid for Scientific Research (20K06820 and 20H03010) to KS, and JSPS Fellowship to HF and AC.

FundersFunder number
JST FORESTJPMJFR2048, 20K06820, 20H03010
Human Frontier Science ProgramRGP0029/2019
Japan Society for the Promotion of Science20K20586
Precursory Research for Embryonic Science and TechnologyJPMJPR16Q6
Moonshot Research and Development ProgramJPNP18016

    Keywords

    • community stability
    • competition
    • dysbiosis
    • ecological niche
    • metabolic interactions
    • microbial functions
    • shotgun metagenomics
    • time-series dynamics

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