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Population genomics of bacterial host adaptation

Abstract

Some bacteria can transfer to new host species, and this poses a risk to human health. Indeed, an estimated 60% of all human pathogens have originated from other animal species. Similarly, human-to-animal transitions are recognized as a major threat to sustainable livestock production, and emerging pathogens impose an increasing burden on crop yield and global food security. Recent advances in high-throughput sequencing technologies have enabled comparative genomic analyses of bacterial populations from multiple hosts. Such studies are providing new insights into the evolutionary processes that underpin the establishment of bacteria in new host niches. A better understanding of the genetic and mechanistic basis for bacterial host adaptation may reveal novel targets for controlling infection or inform the design of approaches to limit the emergence of new pathogens.

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Fig. 1: Host-associated genetic structure in bacterial populations.
Fig. 2: Evolutionary models explaining host-associated population structure.
Fig. 3: The interplay of mutation and recombination in shaping bacterial population structure.
Fig. 4: Genetic mechanisms of bacterial host adaptation.
Fig. 5: Evolutionary scenarios for bacterial host transition and adaptation.

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Acknowledgements

The authors thank current and former members of their laboratories for their contributions to current understanding of this topic. S.K.S. was supported by Medical Research Council (MRC) grants MR/L015080/1 and G0801929, Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/I02464X/1 and the Wellcome Trust. J.R.F. was supported by a project grant (BB/K00638X/1) and institute strategic grant funding BBS/E/D/20002173 from the BBSRC, a Wellcome Trust collaborative award 201531/Z/16/Z and MRC grant MRNO2995X/1. D.S.G. was funded by a Discovery Grant through the Canadian Natural Sciences and Engineering Research Council (NSERC).

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Nature Reviews Genetics thanks D. Dean, M. Polz and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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S.K.S. and J.R.F. researched data for the article, made substantial contributions to discussions of the content and wrote the article. D.S.G. contributed content and reviewed and edited the manuscript before submission.

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Glossary

Effective population size

(Ne). The size of an idealized population that would be reduced in diversity at a rate equal to that of the observed population.

Host adaptation

The ability of bacteria to undergo modification in order to colonize a new host.

Genetic structure

Variation in the genetic makeup of individuals within a population.

Genetic drift

A change in the frequency of an existing gene variant (allele) in a population over time owing to random events (such as mutation).

Ecotypes

Genotypes adapted to a particular niche, which is defined by the extent of spread of an advantageous mutation.

Coalescent theory

A retrospective stochastic genetic model of how genetic diversity arises from a common ancestor.

Phylogroups

A term used in microbiology to describe a deep branching tree structure when monophyletic clades or clonal complexes are difficult to discern.

Linkage disequilibrium

(LD). The nonrandom association of alleles at different loci. LD can be used as a measure of bacterial clonality, which is a lack of recombination that would otherwise disrupt the linkage.

Genetic hitchhiking

The process by which an allele changes frequency in a population because it is linked to a gene under positive selection.

Selective sweep

The fixation of a beneficial allele in a population owing to positive selection, which results in the loss of less fit, alternative alleles.

Core genome

The complement of shared genes among strains of a given bacterial sample or species.

Accessory genome

The complement of strain-dependent (not-shared) genes among strains of a given bacterial sample or species.

Reductive evolution

The downsizing of the genome through gene loss or conversion of genes to pseudogenes.

Genetic bottlenecks

Purges of genetic diversity within a population owing to selective or stochastic events.

Illegitimate recombination

The process by which two non-homologous DNA sequences are joined to each other.

Hill–Robertson effect

The evolutionary advantage provided by recombination when it reduces competition between two beneficial mutations by bringing them into the same genetic background; also known as Hill–Robertson interference.

Clonal interference

Competition between selected clones that carry different competing beneficial mutations.

Pathogenicity islands

Mobile genetic elements containing genes that can confer a pathogenic trait.

Synteny

The physical colocalization and order of loci on the same chromosome in a given strain or species.

Diversifying selection

Selection that occurs when extreme values for a trait are favoured over intermediate values during host adaptation, leading to maintenance of polymorphism (multiple alleles).

Convergent evolution

The independent evolution of similar traits; also known as parallel evolution.

Genome-wide association studies

(GWAS). Studies that use a statistical approach to identify genetic variation within populations that is associated with phenotypic traits.

Epistasis

The interaction between genes whereby the expression of one gene influences the function of another.

Zoonotic

Relating to the transmission of pathogens from animal species to humans.

Gene flow

Transfer of genes from one population to another.

Probabilistic models

Mathematical models used in population genetics to incorporate variables (here, alleles or single nucleotide polymorphisms) and probability distributions (based upon frequency) to identify the number of populations in the sample.

Genetic admixture

The exchange of DNA through recombination between two or more previously isolated populations.

Phylogeographic signatures

Genomic elements that show a segregation pattern that is consistent with geographic distributions of individuals.

Ecological generalism

The capacity to colonize multiple hosts and/or niches.

Metagenomics

The simultaneous analysis of multiple genomes recovered directly from entire bacterial communities, such as environmental or host samples.

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Sheppard, S.K., Guttman, D.S. & Fitzgerald, J.R. Population genomics of bacterial host adaptation. Nat Rev Genet 19, 549–565 (2018). https://doi.org/10.1038/s41576-018-0032-z

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