Metastability transition in genome evolution and population structure of bacterial species
Purushottam Dixit, Columbia University


Multiple evolutionary forces such as point mutation, horizontal gene transfer (HGT), adaptation, and ecological niche separation simultaneously shape genomic diversity within bacterial species. Of these, the interaction between point mutations and HGT is of particular interest as it pertains to a fundamental question: what are bacterial species? On the one hand, binary cell division and vertical inheritance (mother to daughter) of point mutations imposes a clonal population structure. On the other hand, transfer of small genetic fragments between related bacteria corrupts the phylogenetic tree. Whether bacteria can retain clonal phylogeny in the presence of HGT currently remains unknown.

Using a theoretical model, we identify two qualitatively distinct modes of bacterial evolution. In the divergent mode the cohesion due to recombination is not sufficient to overcome vertical inheritance of mutations. As a consequence divergence between genomes increases linearly with time. At the population level, transient clusters of sexually isolated sub-populations are continuously formed and dissolved. The species as a whole retains a clonal population structure. In contrast, in the metastable mode, recombination has the upper hand. Here, genomes remain closely related to each other for very long periods of time before eventually escaping the pull of recombination (hence the name metastable). The population remains genetically cohesive and stable over time. Analysis of real bacteria shows that bacterial species belong to both these modes. Generalizations and future directions are discussed.