Co-evolutionary dynamics of defense systems and anti-defense genes in chromosomes and mobile genetic elements of Enterobacteriaceae

Abstract

Bacterial defense systems undergo rapid evolutionary changes, yet the specific contributions of the genomic compartment (chromosomal versus mobile genetic element [MGE]) to these dynamics remain unclear. We analyzed 6,907 genomes from 213 species of Enterobacteriaceae using a phylogenetic birth-death model to quantify gain, loss, expansion, and reduction of defense (DEF) and anti-defense (anti-DEF) gene families. We found that DEF turnover differs from the background dynamics of the genomic elements that carry them. Direct comparisons among DEFs further revealed differences in loss and copy-number dynamics across genomic compartments, with the highest rates on chromosomes, intermediate rates on plasmids and ICEs/IMEs, and the lowest rates on prophages, whereas the relative balance between gain and loss and between expansion and reduction remained similar across chromosomes and MGEs. MGE-associated anti-DEFs showed higher loss, expansion, and reduction rates than DEFs, whereas chromosome-associated anti-DEFs showed lower gain rates than DEFs. Finally, we found that gains and losses of DEFs and anti-DEFs were positively correlated across bacterial lineages, with positive associations observed for both matching (that is, antagonistic) and non-matching pairs. Together, these results show that genomic background affects the overall flux of DEFs and anti-DEFs, and that turnover of DEFs and anti-DEFs is evolutionarily coupled across lineages.