Shuttling, swapping, and mixing: the rapid modular evolution of antiviral repertoires in temperate phages and their satellites
Abstract
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.
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BibTeX
@article{sousa2026shuttling,
title = {{Shuttling, swapping, and mixing: the rapid modular evolution of antiviral repertoires in temperate phages and their satellites}},
author = {Jorge Moura de Sousa and Florence Depardieu and Marie Touchon and Raphaël Laurenceau and Kristen D Curry and Alice Maestri and Florian Tesson and Arthur Loubat and Rayan Chikhi and Jean Cury and Aude Bernheim and David Bikard and Eduardo P C Rocha},
journal = {Nucleic Acids Research},
year = {2026},
month = sep,
doi = {10.1093/nar/gkag898},
url = {https://hal.science/hal-05764846v1},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Shuttling, swapping, and mixing: the rapid modular evolution of antiviral repertoires in temperate phages and their satellites
AU - Jorge Moura de Sousa
AU - Florence Depardieu
AU - Marie Touchon
AU - Raphaël Laurenceau
AU - Kristen D Curry
AU - Alice Maestri
AU - Florian Tesson
AU - Arthur Loubat
AU - Rayan Chikhi
AU - Jean Cury
AU - Aude Bernheim
AU - David Bikard
AU - Eduardo P C Rocha
PY - 2026
DA - 2026/09/23
JO - Nucleic Acids Research
DO - 10.1093/nar/gkag898
UR - https://hal.science/hal-05764846v1
AB - 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.
SN - 0305-1048
SN - 1362-4962
ER -