Evolutionary dynamics of bacteria in the gut microbiome within and across hosts

Abstract

Gut microbiota are shaped by a combination of ecological and evolutionary forces. While the ecological dynamics have been extensively studied, much less is known about how species of gut bacteria evolve over time. Here, we introduce a model-based framework for quantifying evolutionary dynamics within and across hosts using a panel of metagenomic samples. We use this approach to study evolution in approximately 40 prevalent species in the human gut. Although the patterns of between-host diversity are consistent with quasi-sexual evolution and purifying selection on long timescales, we identify new genealogical signatures that challenge standard population genetic models of these processes. Within hosts, we find that genetic differences that accumulate over 6-month timescales are only rarely attributable to replacement by distantly related strains. Instead, the resident strains more commonly acquire a smaller number of putative evolutionary changes, in which nucleotide variants or gene gains or losses rapidly sweep to high frequency. By comparing these mutations with the typical between-host differences, we find evidence that some sweeps may be seeded by recombination, in addition to new mutations. However, comparisons of adult twins suggest that replacement eventually overwhelms evolution over multi-decade timescales, hinting at fundamental limits to the extent of local adaptation. Together, our results suggest that gut bacteria can evolve on human-relevant timescales, and they highlight the connections between these short-term evolutionary dynamics and longer-term evolution across hosts.

Low Mutational Load Allows for High Mutation Rate Variation in Gut Commensal Bacteria

“…The combination of these two effects could allow strains of the same species to coexist, within the gut microbiota, for extended periods with complex temporal dynamics. The few available data on temporal dynamics of genetic polymorphism in species of human gut commensals is starting to confirm this prediction, at least for some species [5][6][7][8]59]. As genetic diversity can impact community composition [82], more time series data, similar to that obtained here, is needed towards a full understanding of the selective mechanisms that shape the eco-evolutionary dynamics within the microbiota [83,84].…”

“…Moreover, despite the gap in knowledge of the causes of polymorphism in commensal bacteria [57], its high level indicates that deleterious mutations should typically have small effects [58,59]. Remarkably, by analysing polymorphism patterns in species of the human gut microbiome (including E. coli ), Garud et al [5] recently estimated s d / μ = 10 5 ( μ -mutation rate per site). This implies a s d~ 10 -5 , which is fully consistent with our results (with μ = 10 -10 , as estimated for E. coli from mutation accumulation experiments coupled with whole-genome sequencing; [60]).…”

“…[2][3][4]). More recently, it has become clear that there can be abundant genetic diversity within each species colonizing a given individual [5][6][7][8]. Importantly, strain level variation is key for multiple phenotypes ranging from antibiotic resistance and virulence to colonization resistance (e.g.…”

Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration

“…Due to our co-evolution with our gut ecology [31], the gut microbiota's ability to rapidly respond to dietary changes may be reflective of our volatile hunter-gatherer dietary intake that was based on necessity for dietary flexibility with periods of feast and famine [18]. One longitudinal study involving daily gut microbiota investigations of two individuals over the course of a year found that changes in fibre intake are positively correlated with a change in abundance of 15% of the microbial community the following day [5].…”

Toward a dynamical understanding of microbial communities

“…A recent study [31] focused on the most abundant strains from gut microbiomes and limited inquiries to hosts with lineages of bacteria whose genetic structure was simple so that it was possible to assign alleles to a dominant lineage with high confidence. With focus on 40 prevalent species from hundreds of previously published human stool metagenomes-with some samples taken at multiple time points-Garud et al [31] drew numerous inferences concerning evolutionary and ecological dynamics. Many findings are worth noting.…”