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Horizontal gene transfer and adaptive evolution in bacteria

Abstract

Horizontal gene transfer (HGT) is arguably the most conspicuous feature of bacterial evolution. Evidence for HGT is found in most bacterial genomes. Although HGT can considerably alter bacterial genomes, not all transfer events may be biologically significant and may instead represent the outcome of an incessant evolutionary process that only occasionally has a beneficial purpose. When adaptive transfers occur, HGT and positive selection may result in specific, detectable signatures in genomes, such as gene-specific sweeps or increased transfer rates for genes that are ecologically relevant. In this Review, we first discuss the various mechanisms whereby HGT occurs, how the genetic signatures shape patterns of genomic variation and the distinct bioinformatic algorithms developed to detect these patterns. We then discuss the evolutionary theory behind HGT and positive selection in bacteria, and discuss the approaches developed over the past decade to detect transferred DNA that may be involved in adaptation to new environments.

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Fig. 1: Overview of mechanisms of DNA uptake and integration.
Fig. 2: Impacts of allele transfer and gene transfer on genomic variation.
Fig. 3: Evolutionary dynamics that promote gene-specific sweeps.
Fig. 4: Frequencies of genes among members of a bacterial species typically have U-shaped distributions.

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B.J.A. and I-T.H. researched data for the article. B.J.A., W.P.H., and I-T.H. substantially contributed to discussion of content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Brian J. Arnold or William P. Hanage.

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Supplementary information

Glossary

Pangenome

A pangenome consists of a core genome, with genes present in all samples isolates, and an accessory genome, with genes present in only a fraction of sampled isolates.

Reverse ecology

Identifying genomic targets of selection that might provide information on the unknown ecological pressures.

Phages

Viruses that infect bacteria.

Conjugative pilus

Cell-surface appendage that facilitates DNA transfer between bacterial cells.

Integrative conjugative elements

Mobile genetic elements that transfer between cells via conjugation and integrate into bacterial chromosomes, which is in contrast to extracellular plasmids.

Transposable elements

Mobile genetic elements that can duplicate themselves or change positions within bacterial genomes.

Homologous recombination

Protein-mediated genetic exchange between DNA molecules with similar or identical nucleotide sequences.

Linkage

The tendency for nearby mutations in recombining bacteria to be associated with one another due to their being co-inherited across generations. For bacteria that recombine infrequently, mutations in the genome separated by many base pairs will also exhibit substantial linkage.

Haplotype

A particular sequence of linked mutations that are co-inherited or co-transferred between cells.

Speciation

The process by which populations diverge from one another and eventually become distinct named species.

Selfish MGEs

Mobile genetic elements (MGEs) that transfer among genomes with no effect or a negative effect on host fitness. Some elements harbour genes that positively affect host fitness to enhance their transmission.

Convergent evolution

The independent evolution of similar traits in diverged species.

Effective population size

(Ne). The population size that would at equilibrium and under neutral genetic drift exhibit the same genetic diversity as that observed in the sample. This determines the strength of genetic drift and thus the effectiveness of selection.

Gene-specific sweeps

Localized reduction in diversity that is restricted to a specific gene.

Negative frequency-dependent selection

(NFDS). The fitness of a mutation depends negatively on its frequency in the population, such that its fitness decreases as its frequency increases in the population.

Ecotypes

Populations of cells adapted to the same ecological niche.

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Arnold, B.J., Huang, IT. & Hanage, W.P. Horizontal gene transfer and adaptive evolution in bacteria. Nat Rev Microbiol 20, 206–218 (2022). https://doi.org/10.1038/s41579-021-00650-4

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