Of woods and webs: possible alternatives to the tree of life for studying genomic fluidity in <it>E. coli</it>

<p>Abstract</p> <p>Background</p> <p>We introduce several forest-based and network-based methods for exploring microbial evolution, and apply them to the study of thousands of genes from 30 strains of <it>E. coli</it>. This case study illustrates how additional analyses could offer fast heuristic alternatives to standard tree of life (TOL) approaches.</p> <p>Results</p> <p>We use gene networks to identify genes with atypical modes of evolution, and genome networks to characterize the evolution of genetic partnerships between <it>E. coli </it>and mobile genetic elements. We develop a novel polychromatic quartet method to capture patterns of recombination within <it>E. coli</it>, to update the clanistic toolkit, and to search for the impact of lateral gene transfer and of pathogenicity on gene evolution in two large forests of trees bearing <it>E. coli</it>. We unravel high rates of lateral gene transfer involving <it>E. coli </it>(about 40% of the trees under study), and show that both core genes and shell genes of <it>E. coli </it>are affected by non-tree-like evolutionary processes. We show that pathogenic lifestyle impacted the structure of 30% of the gene trees, and that pathogenic strains are more likely to transfer genes with one another than with non-pathogenic strains. In addition, we propose five groups of genes as candidate mobile modules of pathogenicity. We also present strong evidence for recent lateral gene transfer between <it>E. coli </it>and mobile genetic elements.</p> <p>Conclusions</p> <p>Depending on which evolutionary questions biologists want to address (i.e. the identification of modules, genetic partnerships, recombination, lateral gene transfer, or genes with atypical evolutionary modes, etc.), forest-based and network-based methods are preferable to the reconstruction of a single tree, because they provide insights and produce hypotheses about the dynamics of genome evolution, rather than the relative branching order of species and lineages. Such a methodological pluralism - the use of woods and webs - is to be encouraged to analyse the evolutionary processes at play in microbial evolution.</p> <p><it>This manuscript was reviewed by: Ford Doolittle, Tal Pupko, Richard Burian, James McInerney, Didier Raoult, and Yan Boucher</it></p>