Explaining microbial genomic diversity in light of evolutionary ecology

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. Wild populations of bacteria and archaea show high levels of genotypic diversity. In this Review, Cordero and Polz discuss recent studies that show that this diversity arises owing to social and ecological interactions, which have important consequences for microbial ecology and population dynamics. 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 i