Microbial Evolutionary Genomics, Institut Pasteur, CNRS, UMR3525, Paris, France.
Sorbonne Université, Collège doctoral, Paris, France.
PLoS Biol. 2019 Jul 19;17(7):e3000390. doi: 10.1371/journal.pbio.3000390. eCollection 2019 Jul.
Processes of molecular innovation require tinkering and shifting in the function of existing genes. How this occurs in terms of molecular evolution at long evolutionary scales remains poorly understood. Here, we analyse the natural history of a vast group of membrane-associated molecular systems in Bacteria and Archaea-the type IV filament (TFF) superfamily-that diversified in systems involved in flagellar or twitching motility, adhesion, protein secretion, and DNA uptake. The phylogeny of the thousands of detected systems suggests they may have been present in the last universal common ancestor. From there, two lineages-a bacterial and an archaeal-diversified by multiple gene duplications, gene fissions and deletions, and accretion of novel components. Surprisingly, we find that the 'tight adherence' (Tad) systems originated from the interkingdom transfer from Archaea to Bacteria of a system resembling the 'EppA-dependent' (Epd) pilus and were associated with the acquisition of a secretin. The phylogeny and content of ancestral systems suggest that initial bacterial pili were engaged in cell motility and/or DNA uptake. In contrast, specialised protein secretion systems arose several times independently and much later in natural history. The functional diversification of the TFF superfamily was accompanied by genetic rearrangements with implications for genetic regulation and horizontal gene transfer: systems encoded in fewer loci were more frequently exchanged between taxa. This may have contributed to their rapid evolution and spread across Bacteria and Archaea. Hence, the evolutionary history of the superfamily reveals an impressive catalogue of molecular evolution mechanisms that resulted in remarkable functional innovation and specialisation from a relatively small set of components.
分子创新的过程需要对现有基因的功能进行微调和改变。在长期进化尺度上，这种变化在分子进化方面是如何发生的，目前仍知之甚少。在这里，我们分析了细菌和古菌中大量膜相关分子系统的自然史，即第四型丝（TFF）超家族——它们在鞭毛或蠕动运动、粘附、蛋白质分泌和 DNA 摄取系统中多样化。数千个检测到的系统的系统发育表明，它们可能存在于最后一个普遍共同祖先中。从那里，两个谱系——细菌和古菌——通过多次基因复制、基因分裂和缺失以及新成分的积累而多样化。令人惊讶的是，我们发现“紧密附着”（Tad）系统起源于古菌到细菌的跨界转移，类似于“EppA 依赖性”（Epd）菌毛系统，并与分泌系统的获得有关。祖先系统的系统发育和内容表明，最初的细菌菌毛参与了细胞运动和/或 DNA 摄取。相比之下，专门的蛋白质分泌系统在自然历史上出现得更晚，并且多次独立出现。TFF 超家族的功能多样化伴随着遗传重排，这对遗传调控和水平基因转移有影响：在较少的基因座中编码的系统在分类群之间更频繁地交换。这可能促成了它们在细菌和古菌中的快速进化和传播。因此，该超家族的进化历史揭示了一系列令人印象深刻的分子进化机制，这些机制导致了从相对较少的成分中产生了显著的功能创新和专业化。
