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.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.
Highlights
As typical bacterial replicons, circular chromosomes replicate bidirectionally and circular plasmids replicate either bidirectionally or unidirectionally
Our study reveals a definitive example of how an evolutionary transition from unidirectional to bidirectional replication allows the increase of the sizes of chromids, thereby illustrating a process through which plasmids evolve into chromosomes
TAC125 chromid as the standard for unidirectional replication, replication directions were predicted for 16,103 large replicons (.200 kb) out of the total 26,371 replicons from 13,550 genomes
Summary
Circular chromosomes replicate bidirectionally and circular plasmids replicate either bidirectionally or unidirectionally. 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. Prokaryotic DNA replication has been well studied in model bacteria, including the Gram-negative organism Escherichia coli and the Gram-positive organism Bacillus subtilis, both of which have a single circular chromosome that replicates bidirectionally [1,2,3] This bidirectional replication is initiated at the origin (ori) site, after which two replication forks proceed in opposite directions and terminate in the terminus (ter) region, located roughly opposite the ori site on the circular chromosome (see Fig. S1a and b in the supplemental material). A study revealed that the secondary chromosome (Chr2) of the marine bacterium Pseudoalteromonas haloplanktis TAC125 does not show an otherwise expected GC skew, suggesting that it may be replicated unidirectionally [19]
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