Shuttling, swapping, and mixing: the rapid modular evolution of antiviral repertoires in temperate phages and their...

Interactions between bacteria, bacteriophages, and their satellites are shaped by a myriad of defence and counter-defence mechanisms. Here, we identified and characterized the defence hotspots of thousands of P2-like phages and P4-like satellites to elucidate the origins and evolutionary dynamics of defence systems. Both P4 and P2 encode a broad diversity of recognizable defence systems. Defences are a substantial share of the pangenomes, as shown by novel antiviral functions discovered in P4 loci lacking known defence genes. Defence loci are very rapidly swapped, without pseudogenization, suggesting defences are replaced before becoming non-adaptive. This occurs so rapidly that many elements with identical core genes have completely different defences. The intense recombination at hotspots melds components of distinct systems into novel chimeras that were shown to be functional. Surprisingly, P4 and P2 almost never exchange defence genes, despite their simultaneous replication and packaging within cells. In contrast, near-identical defence systems can be found in distinct types of mobile genetic elements and in cryptic chromosomal locations. Our findings highlight P4 and P2 as mobile platforms driving the modular diversification of bacterial antiviral repertoires. Consequently, bacterial defences evolve rapidly through phage and satellite turnover, as well as the swift replacement of defence mechanisms within these elements.