Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/30/2009
Publication Date: 8/11/2009
Citation: Dunn, K.A., Bielawski, J.P., Ward, T.J., Urquhart, C., Gu, H. 2009. Reconciling ecological and genomic divergence among lineages of listeria under an ‘‘extended mosaic genome concept’’. Molecular Biology and Evolution. 26(11):2605-2615.
Interpretive Summary: Listeria monocytogenes is a food-borne bacterium responsible for serious illness in humans and livestock. In recent years, L. monocytogenes has been a leading cause of food recalls and food-borne disease-related deaths. Significant differences in association with human illness have been observed among different strains of L. monocytogenes. These differences can not be explained by the relative frequency of these strains in food products, indicating that some strains have an enhanced ability to cause human illness (pathogen- adapted) while others are better equipped to survive in a variety of non-host environments (generalists). In order to better understand both the genetic basis for these ecological differences and their affects on the Listeria genome, we conducted a genomic analysis of genetic diversity based on complete genome sequences from pathogen adapted, generalist, and non-pathogenic strains of Listeria. Our analyses demonstrated that a large fraction of genes within these genomes have been subject to genetic exchange, while others have evolved differently in pathogen-adapted, generalist, and non-pathogenic Listeria. These results document a group of genes within the Listeria genome that are associated with ecological differences which are of significant interest to public health and the food processing industry.
Technical Abstract: There is growing evidence for a discontinuity between genomic and ecological divergence in several groups of bacteria. Such evidence is difficult to reconcile with the traditional “species genome concept”; i.e., the concept that genomes of ecologically divergent lineages maintain a cohesive gene pool isolated from other gene pools by barriers to homologous recombination. The problem is that bacterial gene pools are not discrete compartments; their member genomes can be porous to exchanges with other gene pools via homologous recombination and lateral gene transfer. There have been several innovative models of bacterial divergence that permit such exchanges; we refer to these, collectively, as “mosaic genome concepts”. These concepts remain a point of contention, as there have been few opportunities to test their most relevant predictions at the genomic scale. Here we undertake such an investigation among ecologically divergent lineages of genus Listeria, and report our assessment of both niche-specific selection pressure and homologous recombination in their core genome. We find evidence of a mosaic Listeria core genome. Some core genes have histories consistent with the expected organism relationships, and have evolved under niche-specific selective pressures. The products of some of those genes can even be linked to metabolic phenotypes with ecological significance. This finding indicates a potentially strong connection between ecological divergence and core genome evolution, and suggests that there can be fitness consequences to exchange of genes among such lineages. In contrast, other core genes appear to have been free to recombine across ecologically divergent lineages or across named species. These findings are hard to reconcile with the traditional species genome concept. Lastly, we suggest that the mosaic genome concepts are themselves idealized models of bacterial genome evolution; their value is that they remind us that named bacterial species do not necessarily represent discrete compartments of biological diversity.