Mazzamurro Fanny, Touchon Marie, Charpentier Xavier, Rocha Eduardo P C
Institut Pasteur, CNRS UMR3525, Microbial Evolutionary Genomics, Université Paris Cité, Paris 75015, France.
Sorbonne Université, Collège Doctoral, Paris F-75005, France.
Mol Biol Evol. 2025 Jul 30;42(8). doi: 10.1093/molbev/msaf192.
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 analyzed 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 turnover in both species. This might result from a negative balance between the transformation's ability to cure the chromosome from mobile genetic elements (MGEs), resulting in gene loss, and its facilitation of gene acquisition. By comparing gene gains by transformation and MGEs, we found that transformation was associated with the acquisition of small sets of genes per event, which were also spread more evenly in the chromosome. We estimated the contribution of natural transformation to gene gains by comparing recombination-driven gene acquisition rates between transformable and non-transformable strains, finding that it facilitated the acquisition of ca. 6.4% (Ab) and 1.1% (Lp) of the novel genes. This moderate contribution of natural transformation to gene acquisition implies that most novel genes are acquired by other means. Yet, 15% of the recently acquired antibiotic resistance genes in A. baumannii may have been acquired by transformation. Hence, natural transformation may drive the acquisition of relatively few novel genes, but these may have a high fitness impact.
自然转化是唯一一种完全由受体细菌控制的基因交换过程。它常常被视为新基因的一个来源，但缺乏对此说法的定量评估。为了研究自然转化在基因获取中的潜在作用，我们分析了一大组鲍曼不动杆菌（Ab）和嗜肺军团菌（Lp）的基因组，这些基因组的转化效率已通过实验测定。自然转化效率与基因组大小的相关性较弱。但在这两个物种中，它们与基因周转率呈负相关。这可能是由于转化从移动遗传元件（MGEs）中清除染色体从而导致基因丢失的能力，与它促进基因获取的能力之间存在负平衡所致。通过比较转化和MGEs带来的基因获得情况，我们发现每次转化事件中，转化与少量基因的获得相关，这些基因在染色体上的分布也更为均匀。我们通过比较可转化菌株和不可转化菌株之间由重组驱动的基因获得率，估算了自然转化对基因获得的贡献，发现它促进了约6.4%（Ab）和1.1%（Lp）的新基因的获得。自然转化对基因获得的这种适度贡献意味着大多数新基因是通过其他方式获得的。然而，鲍曼不动杆菌中最近获得的抗生素抗性基因有15%可能是通过转化获得的。因此，自然转化可能推动了相对较少新基因的获得，但这些基因可能对适应性有很大影响。
