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Evolutionary Trajectory of the Replication Mode of Bacterial Replicons

文献类型: 外文期刊

作者: Xie, Bin-Bin 1 ; Rong, Jin-Cheng 1 ; Tang, Bai-Lu 1 ; Wang, Sishuo 4 ; Liu, Guiming 6 ; Qin, Qi-Long 1 ; Zhang, Xi-Yin 1 ;

作者机构: 1.Shandong Univ, Marine Biotechnol Res Ctr, State Key Lab Microbial Technol, Qingdao, Peoples R China

2.Ocean Univ China, Coll Marine Life Sci & Frontiers Sci, Ctr Deep Ocean Multispheres & Earth Syst, Qingdao, Peoples R China

3.Pilot Natl Lab Marine Sci & Technol Qingdao, Lab Marine Biol & Biotechnol, Qingdao, Peoples R China

4.Chinese Univ Hong Kong, Sch Life Sci, Simon ES Li Marine Sci Lab, Shatin, Hong Kong, Peoples R China

5.Chinese Univ Hong Kong, State Key Lab Agrobiotechnol, Shatin, Hong Kong, Peoples R China

6.Beijing Acad Agr & Forestry Sci, Beijing Agrobiotechnol Res Ctr, Beijing, Peoples R China

7.Univ Warwick, Sch Life Sci, Coventry, W Midlands, England

关键词: chromid; chromosome replication; unidirectional replication; chromosome evolution; Pseudoalteromonas

期刊名称:MBIO ( 影响因子:7.867; 五年影响因子:8.322 )

ISSN: 2150-7511

年卷期: 2021 年 12 卷 1 期

页码:

收录情况: SCI

摘要: 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 Pseudoalteromonas, 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 (ter2) from near the origin site (ori2) 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. IMPORTANCE 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 Pseudoalteromonas 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.

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