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Evolutionary trajectory of the replication mode of bacterial replicons

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Xie, Bin-Bin, Rong, Jin-Cheng, Tang, Bai-Lu, Wang, Sishuo, Liu, Guiming, Qin, Qi-Long, Zhang, Xi-Ying, Zhang, Weipeng, She, Qunxin, Chen, Yin, Li, Fuchuan, Li, Shengying, Chen, Xiu-Lan, Luo, Haiwei, Zhang, Yu-zhong and Cooper, Vaughn S. (2021) Evolutionary trajectory of the replication mode of bacterial replicons. mBio, 12 (1). e02745-20. doi:10.1128/mBio.02745-20

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Official URL: http://dx.doi.org/10.1128/mBio.02745-20

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Abstract

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.

Item Type: Journal Article
Subjects: Q Science > QH Natural history
Divisions: Faculty of Science, Engineering and Medicine > Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Chromosome replication , Plasmids , Bacterial chromosomes
Journal or Publication Title: mBio
Publisher: American Society for Microbiology
ISSN: 2150-7511
Official Date: 26 January 2021
Dates:
DateEvent
26 January 2021Published
1 December 2020Accepted
Volume: 12
Number: 1
Article Number: e02745-20
DOI: 10.1128/mBio.02745-20
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
2016YFA0601303National Key Research and Development Program of ChinaUNSPECIFIED
2018YFC1406700National Key Research and Development Program of ChinaUNSPECIFIED
2018YFC1406702National Key Research and Development Program of ChinaUNSPECIFIED
31630012[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
U1706207[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
31728001[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
91851205[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
31770412[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
42006095[NSFC] National Natural Science Foundation of Chinahttp://dx.doi.org/10.13039/501100001809
AoE/M-403/16Research Grants Council, University Grants Committeehttp://dx.doi.org/10.13039/501100002920

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