Durieux, I. | Search bioRxiv

bioRxiv2023

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.

genomics↗

bioRxiv2019

Diverse conjugative elements silence natural transformation in Legionella species

Natural transformation, i.e. the uptake of DNA and its stable integration in the chromosome, is a major mechanism of horizontal gene transfer and is common in bacteria. The vast majority of bacterial genomes carry the specific genes involved in natural transformation, yet only a fraction of species are deemed naturally transformable. This is typically explained by the inability of standard laboratory conditions to induce this phenotypic trait. However, even when the inducing conditions are known, large intraspecific variations have been reported. In this study, we investigated the conservation and distribution of natural transformability in the human pathogen Legionella pneumophila. Using a panel of 113 clinical isolates, we found that natural transformability is relatively conserved but shows large variations inconsistent with the phylogeny. By conducting a genome-wide association study (GWAS) we identified the conjugative plasmid pLPL as a source of these intraspecific variations. We further show that the plasmid inhibits transformation by simultaneously silencing the genes required for DNA uptake and recombination, comEC, comEA, comF and comM. We identified a plasmid-encoded small RNA (sRNA), RocRp, as solely responsible for the silencing of natural transformation. RocRp is homologous to the highly conserved and chromosome-encoded RocR which controls the transient expression of the DNA uptake system. We show that RocRp can take over the function of RocR, by acting as a substitute, ensuring that the bacterial host of the conjugative plasmid does not become naturally transformable. Distinct homologs of this plasmid-encoded sRNA are found in diverse conjugative elements in other Legionella species, suggesting that silencing natural transformation is beneficial to these genetic elements. We propose that transformation-interfering factors are frequent genetic cargo of mobile genetic elements, accounting for intraspecific variations in natural transformation but also responsible for the apparent non-transformability of some species.

microbiology↗