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  • Review Article
  • Published:

Explaining microbial genomic diversity in light of evolutionary ecology

Nature Reviews Microbiology volume 12, pages 263–273 (2014)Cite this article

Subjects

Key Points

  • Surveys of closely related bacteria and archaea reveal that they have a high degree of genomic diversity, which manifests as single-nucleotide polymorphisms and gene-content variation. To meaningfully interpret the underlying causes of such diversity, it is necessary to clearly define populations — that is, groups of organisms that share a common gene pool and exhibit ecological associations within the same environment and are hence subject to similar selection pressures.

  • High gene frequencies reflect stable selective pressures at the population level, whereas flexible gene content can be partitioned into medium and low gene frequencies to distinguish between different forms of frequency-dependent selection. Such gene categorization enables the generation of hypotheses relating to ecological and evolutionary dynamics.

  • Low-frequency genes often encode different variants of surface structures and have fast rates of turnover, which enables evasion from predators and host immunity; however, the high rate of gene turnover also means that there is low linkage with other genes in the genome, which makes scenarios such as 'kill-the-winner' unlikely explanations for limiting the spread of adaptive clones within populations.

  • Frequency-dependent selection, such as that which arises from social interactions or metabolic trade-offs, can explain the emergence of medium-frequency genes. Moreover, a comparison with animal and plant populations suggests that another role of phenotypic diversity among individuals is population-level synergism, which results from niche complementation.

  • The fact that populations of bacteria and archaea can be regarded as interacting units is also suggested by several studies that have shown asymmetry in the way in which organisms interact within and between populations. Within populations, signalling seems to be increased and antagonism is reduced.

Abstract

Comparisons of closely related microorganisms have shown that individual genomes can be highly diverse in terms of gene content. In this Review, we discuss several studies showing that much of this variation is associated with social and ecological interactions, which have an important role in the population biology of wild populations of bacteria and archaea. These interactions create frequency-dependent selective pressures that can either stabilize gene frequencies at intermediate levels in populations or promote fast gene turnover, which presents as low gene frequencies in genome surveys. Thus, interpretation of gene-content diversity requires the delineation of populations according to cohesive gene flow and ecology, as micro-evolutionary changes arise in response to local selection pressures and population dynamics.

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Figure 1: Gene frequencies and their interpretation in terms of evolutionary and ecological processes.
Figure 2: The role of low gene frequencies and low genetic linkage in bacteria–phage interactions.
Figure 3: Social cheating in natural populations and its role in generating medium-frequency genes.
Figure 4: Asymmetry in intrapopulation versus interpopulation interactions.

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Acknowledgements

The authors wish to thank J. Friedman for valuable discussions. Funding for M.F.P was provided by US National Science Foundation grant DEB 0821391, US National Institute of Environmental Health Sciences grant P30-ES002109, the Moore Foundation and the Broad Institute's Scientific Planning and Allocation of Resources Committee (SPARC) programme.

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Authors and Affiliations

  1. Department of Environmental Systems Science, Swiss Federal Institute of Technology Zurich (ETH-Zürich), Zürich, CH-8092, Switzerland

    Otto X. Cordero

  2. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology (MIT), Cambridge, 02139-4307, Massachusetts, USA

    Martin F. Polz

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  1. Otto X. Cordero
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Correspondence to Otto X. Cordero or Martin F. Polz.

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PowerPoint slides

Glossary

Populations

Groups or clusters of closely related organisms that occupy the same environment and exhibit population-specific gene flow. Although similar to the 'ecotype' concept, populations need only be separated by gene-flow barriers, whereas ecotypes are assumed to contain groups of individuals that have been optimized by selection to occupy a similar niche.

Population bottlenecks

Drastic reductions in the gene pool of a population caused by selective sweeps or demographic fluctuations (for example, few individuals being transmitted during infections).

Sympatry

The coexistence of populations in the same geographic area, such that any gene flow barriers are not caused by geographic isolation but by genetic or behavioural mechanisms.

Clonal sweeps

Reductions of genome-wide variation in clonal populations owing to an increase in the frequency of one genotype that carries an adaptive mutation.

Frequency-dependent selection

A type of selection in which the fitness of a phenotype depends on its frequency in the population.

Genetic linkage

The probability that genes are inherited together. When selection changes the frequency of one gene, it also changes the frequency of the linked genes in a process called hitchhiking.

Gene content

The collection of genes in a genome. At the population level, each gene can be multiallelic.

Flexible genome

The set of genes that are present in only a fraction of the members of a clade.

Core genome

The set of genes that are present in all members of a clade or population.

Niche complementation

The reduction in intraspecies competition among members of a population owing to differences in resource use and interspecies interactions or to ecological facilitation.

Conspecifics

Members of the same species or population.

Niche breadth

The range of environments and resources to which a population is adapted.

Evolvability

The evolutionary potential of a population; that is, the ability of the population to generate novel adaptive mutants.

Microcosms

Experimental assemblages of organisms that are designed to represent simplified models of biological communities.

Negative frequency-dependent selection

A type of frequency-dependent selection that favours rare phenotypes in a population.

Genomic islands

Localized regions in a genome at which horizontal gene transfer and gene loss occur at high rates, resulting in high gene-content diversity at these loci between close relatives.

Public goods

Secreted products that can be used by coexisting bacteria, including cheaters, which do not incur the metabolic cost of production.

Interference competition

A form of competition that involves direct antagonistic interactions between individuals.

Bacteriocins

Proteinaceous toxins produced by bacteria that kill or inhibit the growth of close relatives.

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Cordero, O., Polz, M. Explaining microbial genomic diversity in light of evolutionary ecology. Nat Rev Microbiol 12, 263–273 (2014). https://doi.org/10.1038/nrmicro3218

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