Hülter Nils F, Wein Tanita, Effe Johannes, Garoña Ana, Dagan Tal
Institute of General Microbiology, Kiel University, Kiel, Germany.
Front Microbiol. 2020 Sep 4;11:2062. doi: 10.3389/fmicb.2020.02062. eCollection 2020.
Plasmids are autonomously replicating genetic elements that are ubiquitous in all taxa and habitats where they constitute an integral part of microbial genomes. The stable inheritance of plasmids depends on their segregation during cell division and their long-term persistence in a host population is thought to largely depend on their impact on the host fitness. Nonetheless, many plasmids found in nature are lacking a clear trait that is advantageous to their host; the determinants of plasmid evolutionary success in the absence of plasmid benefit to the host remain understudied. Here we show that stable plasmid inheritance is an important determinant of plasmid evolutionary success. Borrowing terminology from evolutionary biology of cellular living forms, we hypothesize that Darwinian fitness is key for the plasmid evolutionary success. Performing intracellular plasmid competitions between non-mobile plasmids enables us to compare the evolutionary success of plasmid genotypes within the host, i.e., the plasmid fitness. Intracellular head-to-head competitions between stable and unstable variants of the same model plasmid revealed that the stable plasmid variant has a higher fitness in comparison to the unstable plasmid. Preemptive plasmid competitions reveal that plasmid fitness may depend on the order of plasmid arrival in the host. Competitions between plasmids characterized by similar stability of inheritance reveal plasmid fitness differences depending on the plasmid-encoded trait. Our results further reveal that competing plasmids can be maintained in coexistence following plasmid fusions that maintain unstable plasmid variants over time. Plasmids are not only useful accessory genetic elements to their host but they are also evolving and replicating entities, similarly to cellular living forms. There is a clear link between plasmid genetics and plasmid evolutionary success - hence plasmids are evolving entities whose fitness is quantifiable.
质粒是自主复制的遗传元件，在所有生物分类群和栖息地中普遍存在，是微生物基因组的一个组成部分。质粒的稳定遗传取决于它们在细胞分裂过程中的分离，其在宿主群体中的长期存续在很大程度上被认为取决于它们对宿主适应性的影响。尽管如此，自然界中发现的许多质粒缺乏对宿主有利的明确特征；在对宿主无益处的情况下，质粒进化成功的决定因素仍未得到充分研究。在此我们表明，稳定的质粒遗传是质粒进化成功的一个重要决定因素。借鉴细胞生物形式进化生物学的术语，我们假设达尔文适应性是质粒进化成功的关键。在非移动质粒之间进行细胞内质粒竞争，使我们能够比较宿主内质粒基因型的进化成功情况，即质粒适应性。同一模型质粒的稳定和不稳定变体之间的细胞内正面竞争表明，与不稳定质粒相比，稳定质粒变体具有更高的适应性。抢先式质粒竞争表明，质粒适应性可能取决于质粒进入宿主的顺序。具有相似遗传稳定性的质粒之间的竞争揭示了取决于质粒编码特征的质粒适应性差异。我们的结果进一步表明，在随着时间推移维持不稳定质粒变体的质粒融合之后，竞争质粒可以共存。质粒不仅是对其宿主有用的辅助遗传元件，而且它们也是正在进化和复制的实体，类似于细胞生物形式。质粒遗传学与质粒进化成功之间存在明确联系——因此质粒是其适应性可量化的正在进化的实体。
