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Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer

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Simone Pompei, E. Della Bella, Joshua S. Weitz, Jacopo Grilli, Marco Cosentino Lagomarsino

A useful gene can spread through a microbial community without dragging the rest of the genome along with it. This study suggests that separated habitats help explain how diversity survives that takeover.

Abstract

The horizontal transfer of genes is fundamental for the eco-evolutionary dynamics of microbial communities, such as oceanic plankton, soil, and the human microbiome. In the case of an acquired beneficial gene, classic population genetics would predict a genome-wide selective sweep, whereby the genome spreads clonally within the community and together with the beneficial gene, removing genome diversity. Instead, several sources of metagenomic data show the existence of “gene-specific sweeps”, whereby a beneficial gene spreads across a bacterial community, maintaining genome diversity. Several hypotheses have been proposed to explain this process, including the decreasing gene flow between ecologically distant populations, frequency-dependent selection from linked deleterious allelles, and very high rates of horizontal gene transfer. Here, we propose an additional possible scenario grounded in eco-evolutionary principles. Specifically, we show by a mathematical model and simulations that a metacommunity where species can occupy multiple patches, acting together with a realistic (moderate) HGT rate, helps maintain genome diversity. Assuming a scenario of patches dominated by single species, our model predicts that diversity only decreases moderately upon the arrival of a new beneficial gene, and that losses in diversity can be quickly restored. We explore the generic behaviour of diversity as a function of three key parameters, frequency of insertion of new beneficial genes, migration rates and horizontal transfer rates.Our results provides a testable explanation for how diversity can be maintained by gene-specific sweeps even in the absence of high horizontal gene transfer rates.

Transcript

A useful gene can spread through a microbial community without dragging the rest of the genome along with it. This study suggests that separated habitats help explain how diversity survives that takeover. Gene sharing is fundamental for microbial communities in oceanic plankton, soil, and the human microbiome.

When a beneficial gene appears, a simple prediction is that the whole genome carrying it spreads through the community, removing genome diversity. But metagenomic data show a different pattern: a beneficial gene can spread across a bacterial community while genome diversity remains.

This is a gene-specific sweep. The study proposes that many partly separated habitats, together with a moderate rate of gene sharing, can help maintain that diversity. Diversity falls only moderately when a beneficial gene arrives, and lost diversity can be restored quickly.

The central idea is a community spread across many patches, such as separate pockets of nutrients. Think of apartment buildings connected by occasional buses: a popular tenant can move between buildings, but cannot instantly replace everyone everywhere.

Physical separation limits how quickly a beneficial gene can spread through genome migration or horizontal gene transfer across patches. That separation also changes how a selective sweep affects neutral variation across the community, so its impact on other genetic differences can differ from naive expectations.

The model says this patch structure can preserve diversity while the beneficial gene becomes widespread, without requiring extremely frequent reshuffling of genomes. Each patch is treated as supporting one species. The community therefore contains many patches, each usually occupied by a different species, rather than one mixed population everywhere.

Most of the time, each patch is phenotypically uniform, with sporadic, fast selective sweeps replacing what came before with beneficial mutations. So the main question is not whether every patch stays perfectly simple.

It is whether a beneficial gene removes diversity from the community as a whole. The model predicts that its conclusions about maintaining and restoring diversity also hold when several types coexist inside a patch.

The key result is that diversity loss can be moderate when many patches support different species. A beneficial gene does not necessarily erase the community’s variety, because the patches hold different species apart. That result depends on how the different processes unfold over time, with their rates defined separately for each situation.

The picture matters because it links two kinds of change: populations move between connected patches, while a helpful gene can also jump between them. Its spread then reshapes which species remain, as gene carriers grow more likely to take over and others disappear.

When a beneficial gene takes over, diversity drops from roughly eight hundred species to about five hundred rather than disappearing entirely. The loss depends on how the gene spreads: movement between patches removes diversity, while direct gene transfer can preserve it.

A complete takeover of whole genomes occurs only when gene sharing is effectively negligible, so that invasion by the species carrying the beneficial gene is the only important process. As soon as gene sharing is present, more than one species remains after the beneficial gene has spread through the community.

The simulations indicate that a gene-sharing rate ten times slower than the usual movement-and-replacement rate can already restore half of the diversity in the worst-case situation. There is a catch: if new beneficial genes arrive too rapidly, the diversity-restoring process does not have enough time to reach its usual level.

When arrivals are too frequent, the diversity-restoring mechanism does not have enough time to achieve its steady-state diversity in the community. In that regime, the emergence timescale is faster than equilibration, so diversity cannot return to its initial value before recovery is complete.

A beneficial gene can sharply reduce community diversity, but new species gradually restore it; when beneficial genes keep arriving before recovery is complete, diversity stays persistently depressed. This makes the timing of repeated genetic change crucial for biodiversity.

The model is deliberately simple. It leaves out detailed spatial organization, possible links between movement and gene sharing, and much of what happens inside each patch. It also leaves out harmful mutations and competition among several changes inside one population.

Harmful mutations could reduce diversity and alter how long a sweep takes. The result is therefore a time-scale explanation, not a complete description of microbial life; the model deliberately leaves many aspects simplified.

The model's outcomes therefore rely on simple competition between time scales rather than a detailed account of every biological process. When microbes live in many partly separated patches, a beneficial gene can spread while different genomes remain, and moderate gene sharing can help restore lost diversity.

That may help explain the variety found in soil, oceans, and the human microbiome.

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