Intragenomic conflicts with plasmids and chromosomal mobile genetic elements drive the evolution of natural transformation within species

Natural transformation is the only mechanism of genetic exchange controlled by the recipient bacteria. We quantified its rates in 1282 strains of the human pathogens Legionella pneumophila (Lp) and Acinetobacter baumannii (Ab) and found that transformation rates evolve by large quick changes as a jump process across six orders of magnitude. Close to half of the strains are non-transformable in standard conditions. Transitions to non-transformability were frequent and recent, suggesting that they are deleterious and subsequently purged by natural selection. Accordingly, we find that transformation decreases genetic linkage in both species, which often accelerates adaptation. Intragenomic conflicts with chromosomal mobile genetic elements (MGEs) and plasmids could explain these transitions and a GWAS confirmed systematic negative associations between transformation and MGEs: plasmids and other conjugative elements in Lp, prophages in Ab, and transposable elements in both. In accordance with the modulation of transformation rates by genetic conflicts, transformable strains have fewer MGEs. Defense systems against the latter are associated with lower transformation except the adaptive CRISPR-Cas systems which show the inverse trend. The two species have different lifestyles and gene repertoires, but they exhibit very similar trends in terms of variation of transformation rates and its determinants, suggesting that genetic conflicts could drive the evolution of natural transformation in many bacteria.