How Bacterial Lineages Emerge

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Science  06 Apr 2012:
Vol. 336, Issue 6077, pp. 45-46
DOI: 10.1126/science.1219241

Most people today recognize bacterial names like Escherichia coli and Neisseria meningitidis. Yet, from an evolutionary viewpoint, the clarity of species labels for bacteria is blurred by rampant horizontal gene transfer between bacteria (1). The forces driving speciation in bacteria include niche adaptation, selective sweeps, genetic drift, recombination of genetic material, and geographic isolation. How do those forces maintain species homogeneity or bring about lineages, when gene swapping is apparently so rife?

On page 48 of this issue, Shapiro et al. (2) address these questions by providing a high-resolution snapshot of early lineage divergence in marine bacteria. They find clues to the dynamics of prokaryotic genomes, such as with whom the organisms frequently exchange genes, how lineages originate, and, ultimately, what is (or is not) in a name.

Most theoretical and observational insights into what species are and how they came to be are derived from studies of sexually reproducing eukaryotes (3), in which reproduction and recombination are necessarily connected. Asexual lineages in both prokaryotes and eukaryotes have often been described in terms of selection and genomewide genetic linkage, which resets to zero the genetic diversity at every locus (4). However, even though Bacteria and Archaea reproduce asexually, many prokaryotic populations evolve in ways that resemble randomly mating, sexually reproducing eukaryotes: Alleles in these bacterial populations are randomly assorted among individual cells (strains), and diversity at single loci can be purged independently of the other chromosomal loci.

The only mechanism that can explain these observations is a high rate of horizontal gene flow compared to the rates of clonal expansion or reproduction. The main difference from eukaryotes is that prokaryotic reproduction is independent of DNA acquisition and recombination. Instead, DNA is obtained from fragmented chromosomes obtained via parasexual means (that is, without reproduction). These mechanisms of DNA exchange are not restricted to gene exchange within species, and therefore traits can and do come from highly divergent organisms. For example, imagine that acacia trees could exchange DNA with lions and that the resulting new tree developed “limbs” that allowed them to attack grazing giraffes. This is in a sense what prokaryotes do all the time. Very different pathways for bacterial speciation have been described (5, 6); often the data reveal frequent gene flow within multiple exchange groups.

A structured exchange community.

Members of two distinct niches are shown as green and orange squares; gray squares are relatives occupying different niches. Genes that adapt their hosts to these niches are mostly exchanged or recombined between members of the same niche (green and orange arrows), but they might also be shared with recent niche invaders (blue square), accelerating their adaptation to a new habitat. Other genes are freely exchanged between members of different niches (gray arrows). Shapiro et al. show that semi-stable adaptations to specific niches can emerge in the presence of high rates of gene flow within and between lineages.

Horizontal gene flow is thus both a homogenizing and a diversifying force. It typically involves groups of organisms that preferentially exchange genetic material. Mathematical models of gene flow independent of selection and based on sequence similarity alone show that even when rates of relative homologous recombination to mutation are low [in the range of 0.25 to 4 (7)], populations remain recognizably coherent, indicating that selection is not required to give the appearance of delineated species. However, such models do not capture the complexity of gene flow in natural populations. Genetic analysis of closely related strains has shown that genes rarely have the same phylogenetic history (8).

Shapiro et al. now examine the genomes of 20 closely related, yet ecologically differentiated strains of Vibrio cyclitrophicus adapted to living on various-sized particles in the Atlantic Ocean. They find that 99% of the core gene families (which are common to all strains) have different evolutionary histories. Thus, gene acquisition from other lineages, selection on those adaptive alleles, and frequent intraspecies recombination unlinking loci within V. cyclitrophicus have created a thousand-organism chimera. A further indication of vast and frequent gene flow in these asexual organisms comes from pairwise comparisons of genomes. The authors report that in the time it took to accumulate a handful of nucleotide polymorphisms in the core genes, individuals gained reams of new DNA encoding proteins and enzymes that other cells in the population did not have.

These astounding observations reiterate that prokaryotic genomes can be extreme mosaics caused by high rates of gene flow and strong selection. When 99% of genes from a population of very closely related strains do not have the same common ancestor, the only reasonable conclusion is that prokaryotic speciation does not have much to do with divergence from common ancestors—a startling anti-Darwinian outcome.

Surprisingly, in terms of evolutionary outcomes, prokaryotes tend to resemble Darwin's finches. Finches from different species coexisting on the same island become more similar to one another in their overall genome through frequent introgression (incorporation of genetic material via repeated backcrossing of an interspecific hybrid), but the characters defining their ecological niche appear to be maintained through selection.

Genetic exchange groups appear to be the basis of many lineages observed in prokaryotes and are initiated or extinguished by sharing a common spatiotemporal existence with other exchange groups (9, 10). Exchange groups can degenerate through movement to a new habitat or geographic location, or by any mechanism that generates “sexual” isolation, including illegitimately recombined loci (11) and the molecular machinery that shuttles DNA between cells. Perhaps a common mechanism for biasing gene exchange and generating “sexual” isolation is quorum sensing. Many prokaryotes, including pathogens, soil, and marine dwellers, use quorum sensing to regulate gene exchange (12): They only exchange DNA when their numbers dominate in any particular place and time—for example, in a biofilm (13). Quorum sensing is also used by Vibrio populations in biofilms to regulate gene exchange (14). But gene flow regulation does not prohibit divergent DNA from entering or recombining, and exchange groups may be as numerous as potential niches and geographic locations allow.

As Shapiro et al. show, the habitat-specialized Vibrio strains of their study have a gene and niche bias for genetic exchange. Loci that are less important for niche adaptation participate in different and more diverse exchange groups (see the figure). It would seem that the genetic exchange group that has dominated a bacterial population most recently will determine how we observers interpret their evolutionary history of divergence—hopefully while realizing the possibility that newly acquired exchange partners purge evidence of past ones (9, 10). Instead of prokaryotic species having common ancestors, it seems that they are each more like emergent ports-of-call, defined by which genetic vessels are currently moored in their chromosomal harbors.


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