Eco-evolutionary feedbacks in the human gut microbiome

Linking microbial evolution and ecological restructuring in the human gut

Background: The human gut harbors hundreds of microbial species that interact with each other in a complex ecological network. Recent studies have shown that gut microbes can evolve within human-relevant timescales, but little is known about how this evolution impacts (or is impacted by) changes in the local community composition. This study aims to explore the association between short-term microbial evolution and ecological restructuring in the human gut microbiome.

Source: This paper is authored by Benjamin H. Good and Layton B. Rosenfeld from Stanford University, and published in the scientific journal Nature Communications in 2023.

Methods: 1) Study subjects: Metagenomic sequencing data from the Human Microbiome Project, covering over 100 healthy individuals, with 2-3 timepoints per individual spanning approximately 6 months.

2) Analysis pipeline: a) Identify single nucleotide variant (SNV) profiles for each species to determine “strain replacement” (>100 SNV changes) or “evolutionary modification” (<100 SNV changes) events. b) Calculate Jensen-Shannon distances between sample compositions to quantify ecological restructuring between timepoints. c) Test for statistical associations between evolutionary events (replacements/modifications) and ecological distances, and analyze contributing components. d) Construct a simple resource competition model to theoretically investigate the potential for such eco-evolutionary feedbacks.

Key Findings: 1) Different species exhibit significant variation in strain replacement and modification rates, with larger differences at the phylum level (e.g., higher in Firmicutes than Bacteroidetes). 2) Modification events are weakly positively correlated with local diversity, but less than phylum-level differences. 3) Communities undergoing replacements or modifications exhibit significantly larger ecological distances than those without genetic changes. 4) These ecological distance increases cannot be fully explained by changes in core species abundances, often involving non-core, non-phylogenetically related species. 5) Even in a simple resource competition model, beneficial mutations can decrease the relative abundance of their host species and induce coordinated changes in other species.

Significance: 1) Short-term microbial evolution may impact the structure and function of the host microbiome, providing new perspectives for personalized medicine and microbiome engineering. 2) It introduces a new approach to detect eco-evolutionary feedbacks in natural microbial communities, extensible to other complex microbial ecosystems. 3) Theoretical analyses suggest that such feedbacks could arise from simple resource competition dynamics, without invoking other mechanisms (e.g., metabolic exchange, phages).

Novelty: 1) Leveraging large longitudinal datasets, it statistically observes the association between short-term microbial evolution and ecological restructuring in a natural human environment. 2) The analyses reveal that this association often involves changes in non-phylogenetically related species, beyond simple expansion/contraction of the evolving species. 3) Through modeling and theoretical analysis, it proposes that simple resource competition could give rise to similar eco-evolutionary feedbacks.