Similarity of genes horizontally acquired by Escherichia coli and Salmonella enterica is evidence of a supraspecies pangenome

Abstract

Most bacterial and archaeal genomes contain many genes with little or no similarity to other genes, a property that impedes identification of gene origins. By comparing the codon usage of genes shared among strains (primarily vertically inherited genes) and genes unique to one strain (primarily recently horizontally acquired genes), we found that the plurality of unique genes in Escherichia coli and Salmonella enterica are much more similar to each other than are their vertically inherited genes. We conclude that E. coli and S. enterica derive these unique genes from a common source, a supraspecies phylogenetic group that includes the organisms themselves. The phylogenetic range of the sharing appears to include other (but not all) members of the Enterobacteriaceae. We found evidence of similar gene sharing in other bacterial and archaeal taxa. Thus, we conclude that frequent gene exchange, particularly that of genetic novelties, extends well beyond accepted species boundaries.

Fig. 1.

First two axes of a factorial correspondence analysis of the codon usages of E. coli O157:H7 and S. enterica LT2 genes. For each species, colors distinguish shared genes, unique genes, and genes with other distributions (i.e., found in between two and nine strains). Also shown are the modal codon usages of the shared and unique genes of the species.

Fig. 2.

Tree of E. coli and S. enterica modal codon usages. The distances between modal codon usages of the shared and unique genes from all five strains of each species (SI Appendix, Table S2) were used to construct the tree. There are 2,040 shared genes; the number of unique genes follows each genome name. Background colors are the same as in Fig. 1.

Fig. 3.

Interspersion of shared and unique genes on the E. coli O157:H7 and S. enterica LT2 replicons. Each protein coding sequence is colored by its category (shared, unique, or other) and organism, as in Fig. 1.