Review
Omics: Fulfilling the Promise
Ordering microbial diversity into ecologically and genetically cohesive units

https://doi.org/10.1016/j.tim.2014.02.006Get rights and content

Highlights

  • Mathematical models and genomic data provide new insights into microbial speciation.

  • Adaptive genes can either spread within populations or trigger genome-wide sweeps.

  • Formation of new genotypic clusters in sympatry requires (microgeographic) gene flow barriers.

  • If arisen in sympatry, genotypic clusters represent congruent ecological and genetic units.

We propose that microbial diversity must be viewed in light of gene flow and selection, which define units of genetic similarity, and of phenotype and ecological function, respectively. We discuss to what extent ecological and genetic units overlap to form cohesive populations in the wild, based on recent evolutionary modeling and on evidence from some of the first microbial populations studied with genomics. These show that if recombination is frequent and selection moderate, ecologically adaptive mutations or genes can spread within populations independently of their original genomic background (gene-specific sweeps). Alternatively, if the effect of recombination is smaller than selection, genome-wide selective sweeps should occur. In both cases, however, distinct units of overlapping ecological and genotypic similarity will form if microgeographic separation, likely involving ecological tradeoffs, induces barriers to gene flow. These predictions are supported by (meta)genomic data, which suggest that a ‘reverse ecology’ approach, in which genomic and gene flow information is used to make predictions about the nature of ecological units, is a powerful approach to ordering microbial diversity.

Section snippets

Introduction and motivation

It is often said that species are fundamental units of ecology because they comprise individuals that are phenotypically and hence ecologically more similar to each other than to other species 1, 2. This notion was extended in Mayr's biological species concept [3], which states that species are reproductively isolated units, implying that adaptive mutations can spread within a species leaving other coexisting species unaffected. Although recent evidence has shown that reproductive boundaries

Defining genetic and ecological units

Ecological units, in the most basic sense, denote groups of organisms with common ecological functions. It is immediately obvious that this definition represents an abstraction by the observer and is hence subject to individual preferences of how finely one wishes to demarcate units [29]. For example, does the acquisition of an antibiotic resistance gene generate a new ecological unit or simply a variant within an existing unit? Do all sulfate-reducing bacteria represent one ecological unit

Modeling the interplay of selection and recombination

In answering how genotypic clusters originate and are maintained, it is critical to evaluate the interplay of recombination and selection, both of which can vary widely. But although recombination rates can be measured to some extent, the magnitude of selection is difficult to assess directly in the wild, so that we have to rely on reasonable guesses. Below, we give an overview of current knowledge of recombination rates, and then show how mathematical models that explicitly incorporate

Genomics of nascent clusters

As suggested by Wiedenbeck and Cohan [15], detailed investigations of the very early stages of ecological differentiation – whether or not it proceeds to completion – are essential to understanding the interplay of recombination and selection in generating ecological and genetic units. We discuss two such snapshots of slightly different stages in this dynamic process.

In the first, 20 Vibrio cyclitrophicus genomes with identical 16S rRNA genes were sequenced and found to share >99% amino acid

Stages in the speciation spectrum

The snapshots described above suggest a gradual process through which a new niche becomes accessible when novel genes or alleles arise by mutation or HGT in an ancestral population (Table 1, Stage 1). With sufficiently high recombination rates relative to selection, this niche-specifying variant will spread in a gene-specific sweep (Figure 2, Stage 2A). If the new and ancestral niches remain fully sympatric, with no barriers to recombination between them, the process will stop here, as in the

Variation within a cohesive population

Our discussion thus far has focused on how to define and delimit the boundaries between internally cohesive microbial populations. Cohesive populations may nevertheless contain high levels of genotypic (and to some extent, phenotypic) diversity within them. How can this be explained? First, as discussed earlier, niche-specifying variants (genes or alleles) may come with a fitness tradeoff, such that they are adaptive in one niche but not another (indeed, one might even define them as such). In

Concluding remarks and prospects for reverse ecology

As we have outlined in this review, when genotypic clusters can be detected, they should be ecologically differentiated from other such clusters. Although this does not preclude some level of ecological diversity within these clusters due to the potential of acquisition of novel, niche-specifying genes, such diversity should be relatively minor because selection can only maintain a limited number of ecologically divergent loci within the same, genetically mixed population [49]. Hence a reverse

Acknowledgments

We thank Libusha Kelly, Rex Malmstrom, Gabriel Perron, and Rachel Whitaker for their insightful comments. Funding for M.F.P. was provided by National Science Foundation grant DEB 0821391, National Institute of Environmental Health Sciences grant P30-ES002109, the Moore Foundation, and the Broad Institute's Scientific Planning and Allocation of Resources Committee program. Funding for B.J.S. was provided by the Natural Sciences and Engineering Research Council of Canada and the Canada Research

Glossary

Allopatric
a set of sampled isolates or genomes from different geographic areas, where barriers to migration and gene flow are significant.
Clonal frame
the portion of the genome transmitted by vertical (clonal) evolution, unimpacted by HGT. Mutations in the clonal frame should all fall parsimoniously on a single phylogenetic tree.
Core genome
the portion of the genome that is present (or in practice, that can be aligned) in all of a given set of sequenced isolates or metagenomes.
Flexible genome
the

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