Recombinant transfer in the basic genome of Escherichia coli

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 29; pp. 9070 - 9075
• Main Authors: Dixit, Purushottam D, Tin Yau Pang, F. William Studier, Sergei Maslov
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 21-07-2015; National Acad Sciences; Proceedings of the National Academy of Sciences
• Subjects: bacteriophages; Bacteriophages - genetics; Base Pairing - genetics; BASIC BIOLOGICAL SCIENCES; basic genome; Biological Evolution; Biological Sciences; chromosomes; Clone Cells; Cloning; core genome; Deoxyribonucleic acid; DNA; E coli; E. coli evolution; Escherichia coli; Escherichia coli - genetics; Escherichia coli - virology; generalized transduction; Genetic Vectors; genome; Genome, Bacterial; Genomes; homologous recombination; Models, Genetic; Molecular Sequence Annotation; Mosaicism; Mutation; Phylogeny; Polymorphism, Single Nucleotide - genetics; receptors; recombinant transfer; Recombination, Genetic - genetics; Restriction Mapping; Transduction, Genetic; Transformation, Genetic; recombinant transfer; basic genome; E. coli evolution; core genome; generalized transduction
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1510839112

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.
A significant fraction of the length of Escherichia coli genomes comprises mobile elements integrated at various sites in a ∼4-Mbp basic genome shared by the species. We find that the entire basic genome is continually exchanged by homologous recombination with genome fragments acquired from other genomes in the population. Evolutionary groups appear to exchange DNA preferentially within the same group but also with other groups to different extents. Entering DNA is often fragmented by restriction systems of the recipient cell, with surviving pieces replacing homologous parts of the recipient chromosome. Coevolving populations of phages that package genome fragments and deliver them to cells that have appropriate receptors are likely mediators of most DNA transfers, distributing variability throughout the species.