Management of multipartite genomes: the Vibrio cholerae model

Val, Marie-Eve; Soler-Bistué, Alfonso; Bland, M.; Mazel, Didier

doi:10.1016/j.mib.2014.10.003

Cited by 47 publications

(48 citation statements)

References 56 publications

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“…Two basic scenarios for the evolution of multi-chromosomal bacteria have been put forward (61,62). A single large ancestral chromosome could have split into two chromosomes or alternatively, an ancestral strain could have acquired a plasmid, which subsequently acquired essential genes.…”

Section: Discussionmentioning

confidence: 99%

The replication initiator of the cholera pathogen's second chromosome shows structural similarity to plasmid initiators

et al. 2016

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The conserved DnaA-oriC system is used to initiate replication of primary chromosomes throughout the bacterial kingdom; however, bacteria with multipartite genomes evolved distinct systems to initiate replication of secondary chromosomes. In the cholera pathogen, Vibrio cholerae, and in related species, secondary chromosome replication requires the RctB initiator protein. Here, we show that RctB consists of four domains. The structure of its central two domains resembles that of several plasmid replication initiators. RctB contains at least three DNA binding winged-helix-turn-helix motifs, and mutations within any of these severely compromise biological activity. In the structure, RctB adopts a head-to-head dimeric configuration that likely reflects the arrangement in solution. Therefore, major structural reorganization likely accompanies complex formation on the head-to-tail array of binding sites in oriCII. Our findings support the hypothesis that the second Vibrionaceae chromosome arose from an ancestral plasmid, and that RctB may have evolved additional regulatory features.

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Section: Discussionmentioning

confidence: 99%

The replication initiator of the cholera pathogen's second chromosome shows structural similarity to plasmid initiators

et al. 2016

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“…V. cholerae is a model for studying bacteria with multiple chromosomes (20) since it possesses a main chromosome (Chr1) of 2.96 Mbp and a secondary chromosome (Chr2) of 1.07 Mbp. Genome replication starts at the origin of Chr1 ( ori1 ), and the origin of Chr2 ( ori2 ) fires when two-thirds of the larger replicon has been duplicated, finishing their replications synchronously (21, 22).…”

Section: Introductionmentioning

confidence: 99%

The Proximity of Ribosomal Protein Genes to oriC Enhances Vibrio cholerae Fitness in the Absence of Multifork Replication

Soler-Bistué

Michaël

Mazel

2017

mBio

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Recent works suggest that bacterial gene order links chromosome structure to cell homeostasis. Comparative genomics showed that, in fast-growing bacteria, ribosomal protein genes (RP) locate near the replication origin (oriC). We recently showed that Vibrio cholerae employs this positional bias as a growth optimization strategy: under fast-growth conditions, multifork replication increases RP dosage and expression. However, RP location may provide advantages in a dosage-independent manner: for example, the physical proximity of the many ribosomal components, in the context of a crowded cytoplasm, may favor ribosome biogenesis. To uncover putative dosage-independent effects, we studied isogenic V. cholerae derivatives in which the major RP locus, S10-spc-α (S10), was relocated to alternative genomic positions. When bacteria grew fast, bacterial fitness was reduced according to the S10 relative distance to oriC. The growth of wild-type V. cholerae could not be improved by additional copies of the locus, suggesting a physiologically optimized genomic location. Slow growth is expected to uncouple RP position from dosage, since multifork replication does not occur. Under these conditions, we detected a fitness impairment when S10 was far from oriC. Deep sequencing followed by marker frequency analysis in the absence of multifork replication revealed an up to 30% S10 dosage reduction associated with its relocation that closely correlated with fitness alterations. Hence, the impact of S10 location goes beyond a growth optimization strategy during feast periods. RP location may be important during the whole life cycle of this pathogen.

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“…We chose to study three bacterial species with genomes containing multiple circular chromosomes: Vibrio cholerae , Vibrio fischeri , and Burkholderia cenocepacia (19, 21). This is an underappreciated but not uncommon bacterial genome architecture (16, 26–28) and enables effects of chromosome location and replication timing to be distinguished. Setting aside the distinction between chromosomes and megaplasmids (29), the Vibrio cholerae and Vibrio fischeri genomes are composed of two chromosomes, while the Burkholderia cenocepacia genome is composed of three.…”

Section: Introductionmentioning

confidence: 99%

Periodic variation of mutation rates in bacterial genomes associated with replication timing

Dillon

Sung

Lynch³

et al. 2017

Preprint

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34Spontaneous mutation rates may vary within genome regions across the tree of life, but the causes and 35 consequences of this spatiotemporal variation are uncertain because studies of genome-wide mutation 36 rates with sufficient resolution are rare. Here we examine relationships between local mutation rates and 37 replication timing throughout the genomes of three bacterial species using results from five mutation 49would reveal rate periodicity in these experiments. These results support the notion that base-substitution 50 mutation rates are likely to vary systematically across many bacterial genomes, which exposes certain 51 genes to elevated deleterious mutational load.

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Management of multipartite genomes: the Vibrio cholerae model

Cited by 47 publications

References 56 publications

The replication initiator of the cholera pathogen's second chromosome shows structural similarity to plasmid initiators

The replication initiator of the cholera pathogen's second chromosome shows structural similarity to plasmid initiators

The Proximity of Ribosomal Protein Genes to oriC Enhances Vibrio cholerae Fitness in the Absence of Multifork Replication

Periodic variation of mutation rates in bacterial genomes associated with replication timing

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