State Key Laboratory of Microbial Technology, Marine Biotechnology Research Center, Shandong University, Qingdao, China.
College of Marine Life Sciences and Frontiers Science Center for Deep Ocean Multispheres and Earth System, Ocean University of China, Qingdao, China.
mBio. 2021 Jan 26;12(1):e02745-20. doi: 10.1128/mBio.02745-20.
As typical bacterial replicons, circular chromosomes replicate bidirectionally and circular plasmids replicate either bidirectionally or unidirectionally. Whereas the finding of chromids (plasmid-derived chromosomes) in multiple bacterial lineages provides circumstantial evidence that chromosomes likely evolved from plasmids, all experimentally assayed chromids were shown to use bidirectional replication. Here, we employed a model system, the marine bacterial genus , members of which consistently carry a chromosome and a chromid. We provide experimental and bioinformatic evidence that while chromids in a few strains replicate bidirectionally, most replicate unidirectionally. This is the first experimental demonstration of the unidirectional replication mode in bacterial chromids. Phylogenomic and comparative genomic analyses showed that the bidirectional replication evolved only once from a unidirectional ancestor and that this transition was associated with insertions of exogenous DNA and relocation of the replication terminus region () from near the origin site () to a position roughly opposite it. This process enables a plasmid-derived chromosome to increase its size and expand the bacterium's metabolic versatility while keeping its replication synchronized with that of the main chromosome. A major implication of our study is that the uni- and bidirectionally replicating chromids may represent two stages on the evolutionary trajectory from unidirectionally replicating plasmids to bidirectionally replicating chromosomes in bacteria. Further bioinformatic analyses predicted unidirectionally replicating chromids in several unrelated bacterial phyla, suggesting that evolution from unidirectionally to bidirectionally replicating replicons occurred multiple times in bacteria. Chromosome replication is an essential process for cell division. The mode of chromosome replication has important impacts on the structure of the chromosome and replication speed. Bidirectional replication is the rule for bacterial chromosomes, and unidirectional replication has been found only in plasmids. To date, no bacterial chromosomes have been experimentally demonstrated to replicate unidirectionally. Here, we showed that the chromids (plasmid-derived chromosomes) in replicate either uni- or bidirectionally and that a single evolutionary transition from uni- to bidirectionality explains this diversity. These uni- and bidirectionally replicating chromids likely represent two stages during the evolution from a small and unidirectionally replicating plasmid to a large and bidirectionally replicating chromosome. This study provides insights into both the physiology of chromosome replication and the early evolutionary history of bacterial chromosomes.
作为典型的细菌复制子，圆形染色体双向复制，而圆形质粒则双向或单向复制。虽然在多个细菌谱系中发现的质体（质粒衍生的染色体）提供了染色体可能从质粒进化而来的间接证据，但所有经过实验检测的质体都显示出双向复制。在这里，我们采用了一个模型系统，即海洋细菌属，该属的成员始终携带一个染色体和一个质体。我们提供了实验和生物信息学证据，证明尽管少数菌株中的质体双向复制，大多数质体单向复制。这是首次在细菌质体中证明单向复制模式的实验证明。系统发育基因组学和比较基因组学分析表明，双向复制仅从单向祖先进化而来一次，并且这种转变与外源 DNA 的插入和复制终止区域（）从原点附近（）到大致相反位置的重新定位有关。这个过程使质粒衍生的染色体能够增加其大小并扩大细菌的代谢灵活性，同时保持其与主染色体的复制同步。我们研究的一个主要意义是，单向和双向复制的质体可能代表了从单向复制的质粒到细菌中双向复制的染色体的进化轨迹的两个阶段。进一步的生物信息学分析预测了几个不相关细菌门中的单向复制质体，这表明从单向复制到双向复制的复制子的进化在细菌中多次发生。染色体复制是细胞分裂的一个基本过程。染色体复制的模式对染色体的结构和复制速度有重要影响。双向复制是细菌染色体的规则，单向复制仅在质粒中发现。迄今为止，没有实验证明细菌染色体单向复制。在这里，我们表明，在 中复制的质体（质粒衍生的染色体）可以单向或双向复制，并且从单向到双向的单一进化转变解释了这种多样性。这些单向和双向复制的质体可能代表了从一个小的单向复制的质粒到一个大的双向复制的染色体的进化过程中的两个阶段。这项研究为染色体复制的生理学和细菌染色体的早期进化历史提供了新的见解。
