Horizontal gene transfer and the evolution of bacterial and archaeal population structure

Abstract

Many bacterial and archaeal lineages have a history of extensive and ongoing horizontal gene transfer and loss, as evidenced by the large differences in genome content even among otherwise closely related isolates. How ecologically cohesive populations might evolve and be maintained under such conditions of rapid gene turnover has remained controversial. Here we synthesize recent literature demonstrating the importance of habitat and niche in structuring horizontal gene transfer. This leads to a model of ecological speciation via gradual genetic isolation triggered by differential habitat-association of nascent populations. Further, we hypothesize that subpopulations can evolve through local gene-exchange networks by tapping into a gene pool that is adaptive towards local, continuously changing organismic interactions and is, to a large degree, responsible for the observed rapid gene turnover. Overall, these insights help to explain how bacteria and archaea form populations that display both ecological cohesion and high genomic diversity.

Figure 1

Model of the gradual process of genotypic cluster formation via sympatric ecological specialization using the example of an ancestral population associated with zooplankton giving rise to a free-living population in ocean water. In Step 1, at least one genome receives at least one mutation (denoted by green star) via recombination, point mutation or gene loss that adapts it for an alternate habitat. This mutation can spread to other members of the population by recombination. In a phylogenetic tree of a neutral marker gene, the population remains homogeneous. In Step 2, ecological separation is beginning to depress gene flow between the two populations (novel population denoted by green color, which is starting to occupy a niche separate from the zooplankton). The phylogeny still appears mixed because of a history of recombination; only the most recent recombinations show high population-specificity but may not yet be evident in neutral marker genes. Also note that different genes will give different phylogenetic trees due to different degrees of recombination and hitchhiking with the adaptive gene(s). In Step 3, mutations accumulate within each population. Because in bacteria there is an exponential decrease of homologous recombination rate with sequence divergence, this process quickly depresses gene flow between nascent populations. At this point, the phylogenetic tree shows genotypic clusters, which are consistent with ecological differentiation.

Figure 2

Schematic representation of homologous recombination spreading flexible genes among genomes. Comparative genomics increasingly reveals the importance of homologous recombination rather than non-homologous mechanisms in spreading genes among close relatives. This suggests a population-specific gene pool, which can rapidly add or delete genes that are under frequency dependent selection such as the O-antigen or various surface receptors.