Horizontal gene transfer (HGT) promotes the spread of genes within bacterial communities. Among the HGT mechanisms, natural transformation stands out as being encoded by the bacterial core genome. Natural transformation is often viewed as a way to acquire new genes and to generate genetic mixing within bacterial populations. Another recently proposed function is the curing of bacterial genomes of their infectious parasitic mobile genetic elements (MGEs). Here, we propose that these seemingly opposing theoretical points of view can be unified. Although costly for bacterial cells, MGEs can carry functions that are at points in time beneficial to bacteria under stressful conditions (e.g., antibiotic resistance genes). Using computational modeling, we show that, in stochastic environments, an intermediate transformation rate maximizes bacterial fitness by allowing the reversible integration of MGEs carrying resistance genes, although these MGEs are costly for host cell replication. Based on this dual function (MGE acquisition and removal), transformation would be a key mechanism for stabilizing the bacterial genome in the long term, and this would explain its striking conservation.IMPORTANCE Natural transformation is the acquisition, controlled by bacteria, of extracellular DNA and is one of the most common mechanisms of horizontal gene transfer, promoting the spread of resistance genes. However, its evolutionary function remains elusive, and two main roles have been proposed: (i) the new gene acquisition and genetic mixing within bacterial populations and (ii) the removal of infectious parasitic mobile genetic elements (MGEs). While the first one promotes genetic diversification, the other one promotes the removal of foreign DNA and thus genome stability, making these two functions apparently antagonistic. Using a computational model, we show that intermediate transformation rates, commonly observed in bacteria, allow the acquisition then removal of MGEs. The transient acquisition of costly MGEs with resistance genes maximizes bacterial fitness in environments with stochastic stress exposure. Thus, transformation would ensure both a strong dynamic of the bacterial genome in the short term and its long-term stabilization.

中文翻译：

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细菌转化通过可移动遗传元件的可逆整合来缓冲环境波动。

水平基因转移（HGT）促进基因在细菌群落中的传播。在HGT机制中，自然转化突出是由细菌核心基因组编码。自然转化通常被视为获取新基因并在细菌种群中产生遗传混合的一种方式。最近提出的另一个功能是治愈其传染性寄生移动遗传元件（MGE）的细菌基因组。在这里，我们建议可以将这些看似对立的理论观点统一起来。尽管对细菌细胞而言代价高昂，但MGE可以在某些时候发挥一定作用，在压力条件下有益于细菌（例如，抗生素抗性基因）。通过计算建模，我们证明了在随机环境中，中间转化率通过允许携带抗性基因的MGE可逆整合来最大化细菌适应性，尽管这些MGE对于宿主细胞复制而言是昂贵的。基于这种双重功能（MGE的获取和去除），转化将是长期稳定细菌基因组的关键机制，这可以解释其惊人的保守性。重要的自然转化是由细菌控制的细胞外DNA的获取。并且是水平基因转移，促进抗性基因传播的最常见机制之一。但是，其进化功能仍然难以捉摸，并且提出了两个主要作用：（i）细菌种群中的新基因获取和遗传混合，以及（ii）去除传染性寄生移动遗传元件（MGEs）。第一个促进基因多样化，而另一个促进外来DNA的去除，从而促进基因组稳定性，使这两个功能明显具有拮抗作用。使用一个计算模型，我们表明，通常在细菌中观察到的中间转化率允许获得然后去除MGE。瞬时获得具有抗性基因的昂贵MGE可以最大程度提高随机应力暴露环境中的细菌适应性。因此，转化将确保细菌基因组在短期内具有强大的动力，并确保其长期稳定。我们表明，通常在细菌中观察到的中间转化率允许获得然后去除MGE。瞬时获得具有抗性基因的昂贵MGE，可以在具有随机压力的环境中最大限度地提高细菌适应性。因此，转化将确保细菌基因组在短期内具有强大的动力，并确保其长期稳定。我们表明，通常在细菌中观察到的中间转化率允许获得然后去除MGE。瞬时获得具有抗性基因的昂贵MGE，可以在具有随机压力的环境中最大限度地提高细菌适应性。因此，转化将确保细菌基因组在短期内具有强大的动力，并确保其长期稳定。