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  • Review Article
  • Published:

Small change: keeping pace with microevolution

Key Points

  • Bacterial genomes are composed of essential 'core' genes, encoding functions relating to central metabolism and informational processing, and 'accessory' genes that commonly encode supplementary metabolic pathways and virulence factors. 'Foreign' genes in bacterial genomes can be identified by atypical base composition; these might have been imported from quite distant bacterial taxa.

  • Three main tools for examining the microevolution (evolution within species) of bacteria are complete genome sequencing, microarray analysis (which detects changes in gene content) and multi-locus sequencing of 'core' genes. These three approaches have advantages and disadvantages and are most powerfully used in combination.

  • Most bacterial populations consist of a limited number of widespread clonal complexes on the basis of sequence variation in a sample of core genes. These clonal complexes are generally robust with respect to gene choice and are meaningful biological units. These clusters might represent adaptations to specific microniches, and be set on independent evolutionary trajectories.

  • Despite high degrees of clonality, analysis of clonal diversification and phylogenetic approaches examining the relationships between clones both indicate that homologous recombination is an important evolutionary force in many bacterial populations. It is possible that sampling bias leads to an artificially high degree of clonality, but also that the selective origin of clones allows them to withstand the homogenizing effects of recombination.

  • Given the clonal structure of bacterial populations, comparative genomic analysis is most fruitfully carried out with reference to clonal assignments. Such an approach allows a consideration of likely ecological adaptations between isolates and a broad temporal perspective to microevolutionary studies.

Abstract

Bacterial genomes are increasingly viewed in terms of the integration of accessory and dispensable genetic elements into a conserved genomic core. This duality provides both the evolutionary stability that is required for the maintenance of essential functions and the flexibility that is needed for rapid exploitation of new niches. This review focuses on combining genome sequencing, microarray and multilocus sequence data to explore microevolutionary divergence in single species and genera.

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Figure 1: Using eBURST to probe microevolution.
Figure 2: Graph showing sequence diversity compared with allelic diversity from MLST data for S. aureus and S. pneumoniae.

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Acknowledgements

I am very grateful to B. Spratt and M. Holden for critical reading of the manuscript, and for the insightful comments of three anonymous referees. I wish to thank J. Cooper for help with preparing the manuscript. Finally, I am indebted to H. Ochman for guidance and a snappy title. E.J.F. is funded by a Medical Research Council Career Development Award.

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DATABASES

Entrez

Bacillus anthracis

Buchnera aphidicola

Burkholderia cenocepacia

Campylobacter jejuni

Enterococcus faecium

Escherichia coli

Haemophilus influenzae

Helicobacter pylori

Mycobacterium bovis

Mycobacterium tuberculosis

Neisseria meningitidis

Pseudomonas aeruginosa

Shigella sonnei

Staphylococcus aureus

Streptococcus pneumoniae

Streptococcus pyogenes

Vibrio cholerae

Yersinia pestis

FURTHER INFORMATION

eBURST

GENECONV

Genome Atlas database

LDhat

MLST

PLATO

Glossary

MICROEVOLUTION

Commonly defined as any change at or below the level of a single species. As species definition itself is problematic for bacteria, so the boundary between micro- and macro-evolution (between species divergence) is similarly difficult to identify.

TRANSDUCTION

The horizontal transfer of DNA mediated by bacteriophage.

GENOMIC ISLANDS

Clusters of genes that have been imported from unrelated bacterial taxa through lateral gene transfer, and which might help to launch the bacteria into a new (possibly pathogenic) lifestyle. An atypical base composition implicates a 'foreign' origin for these gene clusters, although donor species are rarely, if ever, unequivocally identified.

SYNONYMOUS SUBSTITUTION

A nucleotide change that does not alter the amino acid that is encoded.

TRANSFORMATION

The uptake and incorporation of exogenous ('naked') DNA from lysed cells from the environment.

CLONAL COMPLEX

Sequence types (STs) are grouped into clonal complexes on the basis of sharing a threshold level of allelic identity with at least one other ST in the group (typically five or six identical loci).

CONJUGATION

The transfer of DNA between bacterial cells after cell to cell contact. Conjugation is mediated by mobile genetic elements (usually plasmids or transposons), is unidirectional and conservative (a copy of the DNA remains in the donor strain).

LINKAGE DISEQUILIBRIUM

A situation in which two or more alleles are observed together in a single genome more frequently than expected by chance alone. This might reflect close physical proximity on the chromosome or the absence of recombination between the alleles.

HITCHHIKING EFFECT

The process by which a neutral, or even deleterious, mutation increases in frequency owing to its physical linkage with a beneficial mutation elsewhere in the genome.

FITNESS LANDSCAPE

Multiple populations that have different fitness levels in a bacterial community combine to provide a fitness landscape.

SYMPATRIC

Bacterial populations that occupy the same geographical niche.

MAXIMUM-LIKELIHOOD CONGRUENCE ANALYSIS

A method that selects the phylogenetic tree that has the highest probability of explaining the sequence data, under a specific model of substitution (changes in the nucleotide or amino-acid sequence).

PHYLOGENETIC SIGNAL

The phylogenetic signal is the tendency for related species to resemble each other.

HOMOPLASY

Similarity owing to independent evolutionary changes. For example, an allelic variant, such as a nucleotide variant or a mobile-element insertion at a particular location, that is present in two or more genes, but absent from their common ancestor.

COALESCENT

Relating to the mathematical and statistical properties of genealogies. A modelling framework in which two DNA sequence lineages converge in a common ancestral sequence, going backwards in time.

NON-SYNONYMOUS MUTATION

A change in nucleotide sequence that alters the encoded amino acid.

SPLIT-DECOMPOSITION ANALYSIS

A method that can detect groupings of strains using sequence data that are caused by common ancestry, recombination, convergence, or systematic or random errors. Instead of forcing the sequence data onto a particular tree it produces a networked graph when this is the best representation for the data being analysed.

SEQUENCE SPACE

The universe of all the possible sequences or genotypes. For example, even a small viral genome of 1,000 nucleotides has 3,000 one-step neighbours, nearly 9,000,000 two-step neighbours, and more than 10600 variants at all possible distances of the same genome length.

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Feil, E. Small change: keeping pace with microevolution. Nat Rev Microbiol 2, 483–495 (2004). https://doi.org/10.1038/nrmicro904

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