Selection-driven transcriptome polymorphism in Escherichia coli/Shigella species

Abstract

To explore the role of transcriptome polymorphism in adaptation of organisms to their environment, we evaluated this parameter for the Escherichia coli/Shigella bacterial species, which is composed of well-characterized phylogenetic groups that exhibit characteristic life styles ranging from commensalism to intracellular pathogenicity. Both the genomic content and the transcriptome of 10 strains representative of the major E. coli/Shigella phylogenetic groups were evaluated using macroarrays displaying the 4290 K12-MG1655 open reading frames (ORFs). Although Shigella and enteroinvasive E. coli (EIEC) are not monophyletic, phylogenetic analysis of the binary coded (presence/absence) gene content data showed that these organisms group together due to similar patterns of undetectable K12-MG1655 genes. The variation in transcript abundance was then analyzed using a core genome of 2880 genes present in all strains, after adjusting RNA hybridization signals for DNA hybridization signals. Nonrandom changes in gene expression during the evolution of the E. coli/Shigella species were evidenced. Phylogenetic analysis of transcriptome data again showed that Shigella and EIEC strains group together in terms of gene expression, and this convergence involved groups of genes displaying biologically coherent patterns of functional divergence. Unlike the other E. coli strains evaluated, Shigella and EIEC are intracellular pathogens, and therefore face similar selective pressures. Thus, within the E. coli/Shigella species, strains exhibiting a particular life style have converged toward a specific gene expression pattern in a subset of genes common to the species, revealing the role of selection in shaping transcriptome polymorphism.