Background Escherichia coli O104:H4 caused a severe outbreak in Europe in 2011. The strain TY-2482 sequenced from this outbreak allowed the discovery of its closest relatives but failed to resolve ways in which it originated and evolved. On account of the previous statement, may we expect similar upcoming outbreaks to occur recurrently or spontaneously in the future? The inability to answer these questions shows limitations of the current comparative and evolutionary genomics methods.Principal FindingsThe study revealed oscillations of gene exchange in enterobacteria, which originated from marine γ-Proteobacteria. These mobile genetic elements have become recombination hotspots and effective ‘vehicles’ ensuring a wide distribution of successful combinations of fitness and virulence genes among enterobacteria. Two remarkable peculiarities of the strain TY-2482 and its relatives were observed: i) retaining the genetic primitiveness by these strains as they somehow avoided the main fluxes of horizontal gene transfer which effectively penetrated other enetrobacteria; ii) acquisition of antibiotic resistance genes in a plasmid genomic island of β-Proteobacteria origin which ontologically is unrelated to the predominant genomic islands of enterobacteria.ConclusionsOscillations of horizontal gene exchange activity were reported which result from a counterbalance between the acquired resistance of bacteria towards existing mobile vectors and the generation of new vectors in the environmental microflora. We hypothesized that TY-2482 may originate from a genetically primitive lineage of E. coli that has evolved in confined geographical areas and brought by human migration or cattle trade onto an intersection of several independent streams of horizontal gene exchange. Development of a system for monitoring the new and most active gene exchange events was proposed.

With more sequences of complete bacterial genomes getting public availability the approaches of genome comparison by frequencies of oligonucleotides (k-mers) known also as the genome linguistics are becoming popular and practical to resolve problems which can not be tackled by the traditional sequence comparison tools. In this work we present several innovative approaches based on k-mer statistics for detection of inserts of genomic islands and tracing down the ontological links and origins of mobile genetic elements. 637 bacterial genomes were analyzed by SeqWord Sniffer program that has detected 2,622 putative genomic islands. These genomic islands were clustered by DNA compositional similarity. A stratigraphic analysis was introduced that allows distinguishing between new and old genomic inserts. A method of reconstruction of donor-recipient relations between microorganisms was proposed. The strain E. coli TY-2,482 isolated from the latest deadly outbreak of a haemorrhagic infection in Europe in 2011 was used for the case study. It was shown that this strain appeared on an intersection of two independent fluxes of horizontal gene exchange, one of which is a conventional for Enterobacteria stream of vectors generated in marine gamma-Proteobacteria; and the second is a new channel of antibiotic resistance genomic islands originated from environmental beta-Proteobacteria.