Biology subjects

Mazzamurro, F.

Publications and source records attributed to Mazzamurro, F..

4 recordsLinked to original sources

bioRxiv2025

Impact of natural transformation on the acquisition of novel genes in bacteria

Natural transformation is the only process of gene exchange under the exclusive control of the recipient bacteria. It has often been considered as a source of novel genes but quantitative assessments of this claim are lacking. To investigate the potential role of natural transformation in gene acquisition, we analysed a large collection of genomes of Acinetobacter baumannii (Ab) and Legionella pneumophila (Lp) for which transformation rates were experimentally determined. Natural transformation rates are weakly correlated with genome size. But they are negatively associated with gene flow in both species. This might result from a negative balance between transformations ability to cure the chromosome from mobile genetic elements (MGEs), resulting in gene loss, and its facilitation of gene acquisition. By focusing on the latter, we found that transformation was significantly associated with small gene acquisition events while MGEs-driven gene acquisition tend to be associated with larger ones. Events of gene gain by transformation were spread more evenly in the chromosome than MGEs encoding the ability to integrate autonomously. We estimated the contribution of natural transformation to gene gains by comparing recombination-driven gene acquisition rates between transformable and non-transformable strains. Natural transformation may have caused the acquisition of up to 6.4% (Ab) and 1.1% (Lp) of the novel genes. This low contribution of natural transformation to the acquisition of novel genes implies that most novel genes must have been acquired by other means. Interestingly, the ones potentially acquired by transformation include almost 15% of the recently acquired antibiotic resistance genes in A. baumannii. Hence, natural transformation may drive the acquisition of relatively few novel genes but these may have a high fitness impact.

genomics↗

bioRxiv2024

YraN is a helicase-associated nuclease fostering extended recombination events by natural transformation

Natural transformation is a widespread mechanism driving genetic exchanges in bacteria. It proceeds by the capture and internalization of exogenous DNA in linear single strands, ultimately integrated in the genome by homologous recombination. It is unknown how the RecA-directed D-loop intermediate of this dedicated recombination pathway is processed. We report that resolution of the transformation D-loop depends on two endonucleases of opposing phylogenetic distribution in bacteria. One is YraN, which has co-evolved and interacts with the ComM helicase, known to extend DNA recombination at the transformation D-loop. The other is CoiA, which is restricted to the Bacillota. CoiA is shown to be a resolvase of the transformation D-loop, extended by the RadA helicase in these species. We demonstrate that both YraN and CoiA act synergistically with their cognate helicases. These findings reveal that bacteria have evolved two helicase/nuclease pairs for the maturation and recombination extension of the transformation D-loop.

microbiology↗

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↗

bioRxiv2023

Chance favors the prepared genomes: horizontal transfer shapes the emergence of antibiotic resistance mutations in core genes.

Bacterial lineages vary in the frequency with which they acquire novel traits, like antibiotic resistance or virulence. While previous studies have highlighted the impact of the genetic background on the successful acquisition of novel traits through horizontal gene transfer, the impact of the latter on the subsequent evolution of bacterial genomes by point mutations remains poorly understood. Here, we studied the evolution of resistance to quinolones in thousands of Escherichia coli genomes. Resistance-conferring point mutations in the core genes are frequent and accumulate very quickly. We searched for gene gains and losses significantly associated with the subsequent acquisition of these resistance mutations. This revealed 60 groups of genes in genetic linkage whose gain or loss induced a change in the probability of subsequently becoming resistant to quinolones by point mutations in gyrA and parC. Although some of these chronologies may reflect epidemiological trends, most of these groups encoded functions that were previously associated with antibiotic resistance, tolerance, or persistence, often specifically under quinolone treatment. A lot of the largest groups were found in prophages or plasmids, and they usually increased the likelihood of subsequent resistance mutations. Conversely groups of lost genes were typically small and chromosomal. Quinolone resistance was among the first resistances acquired in the extant lineages of E. coli and its acquisition was associated with an increased likelihood of acquiring other types of resistances, including to aminoglycosides and beta-lactams. Our findings suggest that gene flow shapes the subsequent fixation rate of adaptive mutations in core genes. Given the substantial gene flow within bacterial genomes, interactions between horizontal transfer and point mutations in core genes may be key to the success of adaptation processes.

evolutionary biology↗