Molecular archaeology of the Escherichia coli genome

Abstract

The availability of the complete sequence of Escherichia coli strain MG1655 provides the first opportunity to assess the overall impact of horizontal genetic transfer on the evolution of bacterial genomes. We found that 755 of 4,288 ORFs (547.8 kb) have been introduced into the E. coli genome in at least 234 lateral transfer events since this species diverged from the Salmonella lineage 100 million years (Myr) ago. The average age of introduced genes was 14.4 Myr, yielding a rate of transfer 16 kb/Myr/lineage since divergence. Although most of the acquired genes subsequently were deleted, the sequences that have persisted ( approximately 18% of the current chromosome) have conferred properties permitting E. coli to explore otherwise unreachable ecological niches.

Figure 1

Distribution of horizontally transferred DNA in the E. coli MG1655 chromosome. Within each centisome, each bar denotes a continuous segment of transferred DNA containing one or more ORFs; and the length of each bar represents its size rounded to the nearest 500 bp. Features of transferred regions, such as duration in the chromosome and the identification of repeated and mobile elements, follow the notation presented in the key. The age of each continuous segment of DNA was inferred from the ages of genes successfully analyzed by back-amelioration; segments lacking genes of known age are shown in black, and no segment comprised genes with significantly different ages. Positions of the replication origin (oriC) and terminus (terC), as well as the identity of the specific tRNA loci found to be adjacent to a horizontally transferred region, are noted on the left of the open bar representing the MG1655 chromosome. The nomenclature for phage and IS elements, and for genes of known function contained within a particular transferred segment, are shown within the corresponding bar. The identities of insertion sequences are noted except as follows: adjacent IS911/(fragment)/IS3 are located within minute 5; adjacent IS3/IS600 are located within minute 8; and adjacent IS2/IS30 are located within minute 31.

Figure 2

Age distribution of horizontally transferred DNA in the E. coli MG1655 chromosome. Bars represent the amount of protein-coding, horizontally transferred DNA of the specified age present in the 571 genes analyzed by back amelioration. The remaining 184 genes could not be successfully analyzed because of aberrant nucleotide compositions, which could result from horizontal transfer among more than one genome; most of the genes comprising this group are encoded by prophages and mobile genetic elements.