Recombinant transfer in the basic genome of Escherichia coli

Abstract

An approximation to the ∼4-Mbp basic genome shared by 32 strains of Escherichia coli representing six evolutionary groups has been derived and analyzed computationally. A multiple alignment of the 32 complete genome sequences was filtered to remove mobile elements and identify the most reliable ∼90% of the aligned length of each of the resulting 496 basic-genome pairs. Patterns of single base-pair mutations (SNPs) in aligned pairs distinguish clonally inherited regions from regions where either genome has acquired DNA fragments from diverged genomes by homologous recombination since their last common ancestor. Such recombinant transfer is pervasive across the basic genome, mostly between genomes in the same evolutionary group, and generates many unique mosaic patterns. The six least-diverged genome pairs have one or two recombinant transfers of length ∼40-115 kbp (and few if any other transfers), each containing one or more gene clusters known to confer strong selective advantage in some environments. Moderately diverged genome pairs (0.4-1% SNPs) show mosaic patterns of interspersed clonal and recombinant regions of varying lengths throughout the basic genome, whereas more highly diverged pairs within an evolutionary group or pairs between evolutionary groups having >1.3% SNPs have few clonal matches longer than a few kilobase pairs. Many recombinant transfers appear to incorporate fragments of the entering DNA produced by restriction systems of the recipient cell. A simple computational model can closely fit the data. Most recombinant transfers seem likely to be due to generalized transduction by coevolving populations of phages, which could efficiently distribute variability throughout bacterial genomes.

Keywords: E. coli evolution; basic genome; core genome; generalized transduction; recombinant transfer.

Fig. 1.

Phylogenetic tree derived from filtered genome-wide average SNP densities (Δ) between 496 pairs of 32 basic genomes. Previously recognized phylogenetic groups: E (light blue), A (green), B1 (blue), D2 (yellow), D1 (brown), and B2 (red). The tree was calculated using UPGMA algorithm. Dots in the lines connecting pairs of evolutionary groups are placed approximately at average SNP densities between them. The groups are ordered to fit the relative divergences among them summarized in Table S1. GenBank accession numbers are given in Table S3.

Fig. S1.

Distribution of the 3,903 basic-genome segments of 1 kbp as a function of cumulative SNP density in the filtered 32-strain basic-genome alignment (δ_cum is the percentage of aligned base pair positions having a SNP in any strain). An approximately normal distribution of 3,769 segments with δ_cum = 0.3–18.0%, average of 7.5%, is followed by a scattered tail of 134 segments with δ_cum = 18.1–60.2%, average of 29.1%.

Fig. 2.

Distributions of SNP densities between basic genomes. (A) Distribution of perfectly aligned 1-kbp segments from the set of 3,769 as a function of average SNP density δ for five basic-genome pairs: group A strain MG1655 aligned with ETEC (A–A, Δ = 0.38%, black triangles); B–DL (A–A, Δ = 0.72%, brown squares); SE11 (A–B1, Δ = 1.16%, red triangles); O157 (A–E, Δ = 1.56%, blue circles); and IHE (A–B2, Δ = 2.54%, green diamonds). (B) Distributions of SNP density as a function of δ as predicted by the computational model given in Supporting Information for pairs of genomes having the same average SNP densities Δ as the five genome pairs in A.

Fig. 3.

Values of clonal fraction, Δ_c, and Δ_t as a function of overall divergence Δ in 496 basic-genome pairs. (A) Clonal fraction f_c; (B) average SNP density in the clonal fraction Δ_c; (C) average SNP density in the transferred fraction Δ_t. Data points for genome pairs within evolutionary groups A are given by solid green circles; B1 by blue squares; B2 by red diamonds; between A and B1 by violet asterisks; and other pairs by a black X. Dashed red lines with error bars are values predicted by the computational model given in Supporting Information. Error bars correspond to SD of 100 runs of the model.

Fig. 4.

Average lengths of clonal and transferred regions, and numbers of each as a function of overall divergence Δ in 496 basic-genome pairs. (A) Average lengths of clonal regions (in kilobase pairs); (B) average lengths of transferred regions (in kilobase pairs); (C) number of transferred regions (equal numbers of interspersed clonal and transferred regions). Data points, dashed red lines, and error bars are as in Fig. 3.