Wein Tanita, Wang Yiqing, Hülter Nils F, Hammerschmidt Katrin, Dagan Tal
Institute of Microbiology, Kiel University, Am Botanischen Garten 11, 24118 Kiel, Germany.
Institute of Microbiology, Kiel University, Am Botanischen Garten 11, 24118 Kiel, Germany.
Curr Biol. 2020 Oct 5;30(19):3841-3847.e4. doi: 10.1016/j.cub.2020.07.019. Epub 2020 Aug 13.
Extra-chromosomal genetic elements are important drivers of bacterial evolution, and their evolutionary success depends on positive selection for the genes they encode. Examples are plasmids encoding antibiotic resistance genes that are maintained in the presence of antibiotics (e.g., [1-3]). Plasmid maintenance is considered a metabolic burden to the host [4]; hence, when the cost of plasmid carriage outweighs its benefit, plasmid-free segregants are expected to outcompete plasmid-carrying cells, eventually leading to plasmid loss [5-7]. Thus, in the absence of positive selection, plasmid survival hinges upon stable persistence in the population. The ubiquity of plasmids in nature suggests that plasmids having a negligible effect on host fitness may evolve stable inheritance and thus gain a long-term persistence in the population, also in the absence of positive selection [8]. Nonetheless, the transition of plasmids into stably inherited genetic elements remains understudied. Here, we show that positive selection for a plasmid-encoded gene interferes with the evolution of plasmid stability. Evolving plasmids under different selection regimes in Escherichia coli, we find that antibiotics led to plasmid amplification, resulting in plasmid instability. Thus, under positive selection, suboptimal solutions for plasmid stability were maintained in the population hindering long-term plasmid persistence. Indeed, a survey of Escherichia plasmids confirms that antibiotic resistance genes are rarely found on small plasmids. Our results show that a plasmid-mediated advantage for the host may manifest in reduced plasmid evolutionary success. Considering plasmids as autonomously evolving entities holds promise for understanding the factors that govern their evolution.
染色体外遗传元件是细菌进化的重要驱动因素，它们的进化成功取决于对其所编码基因的正选择。例如，编码抗生素抗性基因的质粒在抗生素存在的情况下得以维持（例如，[1 - 3]）。质粒维持被认为是宿主的一种代谢负担[4]；因此，当携带质粒的成本超过其益处时，预计无质粒的分离株将比携带质粒的细胞更具竞争力，最终导致质粒丢失[5 - 7]。因此，在没有正选择的情况下，质粒的存活取决于在群体中的稳定存续。自然界中质粒的普遍存在表明，对宿主适应性影响可忽略不计的质粒可能进化出稳定的遗传方式，从而在群体中实现长期存续，即便在没有正选择的情况下也是如此[8]。尽管如此，质粒向稳定遗传元件的转变仍未得到充分研究。在这里，我们表明对质粒编码基因的正选择会干扰质粒稳定性的进化。在大肠杆菌中于不同选择条件下培养质粒，我们发现抗生素导致质粒扩增，进而导致质粒不稳定。因此，在正选择下，群体中维持着质粒稳定性的次优解决方案，这阻碍了质粒的长期存续。事实上，对大肠杆菌质粒的一项调查证实，抗生素抗性基因很少出现在小质粒上。我们的结果表明，质粒介导的对宿主的优势可能表现为质粒进化成功率降低。将质粒视为自主进化的实体有助于理解控制其进化的因素。
