Fate of the H-NS–Repressed bgl Operon in Evolution of Escherichia coli

Abstract

In the enterobacterial species Escherichia coli and Salmonella enterica, expression of horizontally acquired genes with a higher than average AT content is repressed by the nucleoid-associated protein H-NS. A classical example of an H-NS–repressed locus is the bgl (aryl-β,D-glucoside) operon of E. coli. This locus is “cryptic,” as no laboratory growth conditions are known to relieve repression of bgl by H-NS in E. coli K12. However, repression can be relieved by spontaneous mutations. Here, we investigated the phylogeny of the bgl operon. Typing of bgl in a representative collection of E. coli demonstrated that it evolved clonally and that it is present in strains of the phylogenetic groups A, B1, and B2, while it is presumably replaced by a cluster of ORFans in the phylogenetic group D. Interestingly, the bgl operon is mutated in 20% of the strains of phylogenetic groups A and B1, suggesting erosion of bgl in these groups. However, bgl is functional in almost all B2 isolates and, in approximately 50% of them, it is weakly expressed at laboratory growth conditions. Homologs of bgl genes exist in Klebsiella, Enterobacter, and Erwinia species and also in low GC-content Gram-positive bacteria, while absent in E. albertii and Salmonella sp. This suggests horizontal transfer of bgl genes to an ancestral Enterobacterium. Conservation and weak expression of bgl in isolates of phylogenetic group B2 may indicate a functional role of bgl in extraintestinal pathogenic E. coli.

Author Summary

Horizontal gene transfer, an important mechanism in bacterial adaptation and evolution, requires mechanisms to avoid uncontrolled and possibly disadvantageous expression of the transferred genes. Recently, it was shown that the protein H-NS selectively silences genes gained by horizontal transfer in enteric bacteria. Regulated expression of these genes can then evolve and be integrated into the regulatory network of the new host. Our analysis of the catabolic bgl (aryl-β,D-glucoside) operon, which is silenced by H-NS in E. coli, provides a snapshot on the evolution of such a locus. Genes of the bgl operon were presumably gained by horizontal transfer from Gram-positive bacteria to ancestral enteric bacteria. In E. coli, the bgl operon co-evolved with the diversification of the species into four phylogenetic groups. In one phylogenetic group the bgl operon is functional. However, in two other phylogenetic groups, bgl accumulates disrupting mutations, and it is absent in the fourth group. This indicates that the H-NS–silenced bgl operon evolved differently in E. coli and is presumably positively selected in one phylogenetic group, while it is neutrally or negatively selected in the other groups.