Establishing a new paradigm in bacterial evolution: chromosomal hypermobility via lateral transduction

Phage-mediated gene transfer is a major evolutionary force. It occurs by two well-described mechanisms: generalised and specialised transduction. We have discovered that Staphylococcus aureus pac phages engage in lateral transduction (LT), the most powerful mode of transduction described to date. LT converts large regions of the bacterial chromosome into "hypermobile platforms" for the high frequency transfer of any genetic element within their boundaries. Bacterial DNA is transferred at astonishingly high frequencies that are at least 1,000 times greater than any known mechanism of transduction. The observed efficiency of chromosomal DNA transfer is unprecedented, representing a paradigm shift in phage biology and in the definition of mobile genetic elements. Importantly, two recent unpublished discoveries from the lab highlight the existence of additional mechanisms of gene transfer, related to LT, which require investigation. Although it's assumed that cos phages can't transduce DNA, our results indicate that they engage in a new form of LT that we have called cos-LT. We have also discovered that a large family of pathogenicity islands, the phage-inducible chromosomal islands (PICIs), promote the transfer of chromosomal genes by a related mechanism of transduction termed PICI-LT. Importantly, PICI-LT has unique mechanistic features suggesting it may be even more frequent and powerful than LT. Here, analysing selected diverse major pathogens, we'll investigate how widespread these ground-breaking strategies of gene transfer (LT, PICI-LT and cos-LT) are in nature, along with their impact on the structure of bacterial genomes, and the evolution of virulence and antimicrobial resistance. Furthermore, the environmental drivers of LT, PICI-LT and cos-LT among bacterial communities will be examined in models of distinct ecological habitats. The proposed research will require a major revision of our understanding of the impact of phages and PICIs on bacterial evolution.