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Vibrio chromosomes share common history.

Kirkup BC, Chang L, Chang S, Gevers D, Polz MF - BMC Microbiol. (2010)

Bottom Line: Single copy genes from each chromosome (142 genes from chromosome I and 42 genes from chromosome II) were identified from 19 sequenced Vibrionales genomes and their phylogenetic comparison suggests consistent phylogenies for each chromosome.Additionally, study of the gene organization and phylogeny of the respective origins of replication confirmed the shared history.Thus, while elements within the chromosomes may have experienced significant genetic mobility, the backbones share a common history.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dept, of Civil and Environmental Engineering, 15 Vassar Street, Cambridge, MA 02139, USA. bckirkup@post.harvard.edu

ABSTRACT

Background: While most gamma proteobacteria have a single circular chromosome, Vibrionales have two circular chromosomes. Horizontal gene transfer is common among Vibrios, and in light of this genetic mobility, it is an open question to what extent the two chromosomes themselves share a common history since their formation.

Results: Single copy genes from each chromosome (142 genes from chromosome I and 42 genes from chromosome II) were identified from 19 sequenced Vibrionales genomes and their phylogenetic comparison suggests consistent phylogenies for each chromosome. Additionally, study of the gene organization and phylogeny of the respective origins of replication confirmed the shared history.

Conclusions: Thus, while elements within the chromosomes may have experienced significant genetic mobility, the backbones share a common history. This allows conclusions based on multilocus sequence analysis (MLSA) for one chromosome to be applied equally to both chromosomes.

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OriI and OriII synteny figures. The two origin regions of (A) Chromosome I and (B) Chromosome II. Open reading frames called in the annotated genomes are polygons pointing in the direction of their orientation. Colors label the open reading frames analyzed individually in estimating the phylogeny of the origin. The expanded figures with all labels are found in Additional files 3 and 4, supplementary materials.
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Figure 3: OriI and OriII synteny figures. The two origin regions of (A) Chromosome I and (B) Chromosome II. Open reading frames called in the annotated genomes are polygons pointing in the direction of their orientation. Colors label the open reading frames analyzed individually in estimating the phylogeny of the origin. The expanded figures with all labels are found in Additional files 3 and 4, supplementary materials.

Mentions: The second method of analysis, studying the gene organization at the origins of replication (Ori), supported the finding that the two chromosomes share a single phylogeny at the species level. This method of analysis was more advantageously applied to chromosome II than chromosome I: Gene order in the region immediately surrounding the chromosome I origin appears too highly conserved between species to provide robust data on its phylogeny (Figure 3; expanded in Additional files 3 and 4). However, gene content is informative in that region suggesting that the species largely conform to the expected clustering even though the tree is not well supported (Figure 3). The difficulties are caused by a paucity of organizational changes that differentiate species at OriI - such as the inversion of three genes that sets apart the V. fisheri. Frequently, a change is unique to a sequenced strain and not shared by other members of its species. This can be extraordinarily disruptive of a distance estimate if the number of unique differences is large. In particular, at least three obvious saltations in the gene content introduce spikes of noise. In V. cholerae B33, an apparently mobile genetic region has imposed itself very close to the origin of replication. These 18 genes, almost as large as the region to be compared, interrupt an otherwise absolutely conserved region shared by the other Vibrio cholerae. A 9 gene region in Photobacterium sp. SKA34 contains several transposon and transposase genes. Similarly, 16 gene region in Vibrio splendidus MED222 interrupts an otherwise conserved region with a number of secretory system genes; it lacks apparent mobility elements which would explain its origin. Among the photobacteria, the flanking regions sometimes differ dramatically, as well, which disturbs the phylogeny with a very long branch, and the Vibrio cholerae appear to have inverted the entire region - but this would not impact a gene content analysis.


Vibrio chromosomes share common history.

Kirkup BC, Chang L, Chang S, Gevers D, Polz MF - BMC Microbiol. (2010)

OriI and OriII synteny figures. The two origin regions of (A) Chromosome I and (B) Chromosome II. Open reading frames called in the annotated genomes are polygons pointing in the direction of their orientation. Colors label the open reading frames analyzed individually in estimating the phylogeny of the origin. The expanded figures with all labels are found in Additional files 3 and 4, supplementary materials.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2875227&req=5

Figure 3: OriI and OriII synteny figures. The two origin regions of (A) Chromosome I and (B) Chromosome II. Open reading frames called in the annotated genomes are polygons pointing in the direction of their orientation. Colors label the open reading frames analyzed individually in estimating the phylogeny of the origin. The expanded figures with all labels are found in Additional files 3 and 4, supplementary materials.
Mentions: The second method of analysis, studying the gene organization at the origins of replication (Ori), supported the finding that the two chromosomes share a single phylogeny at the species level. This method of analysis was more advantageously applied to chromosome II than chromosome I: Gene order in the region immediately surrounding the chromosome I origin appears too highly conserved between species to provide robust data on its phylogeny (Figure 3; expanded in Additional files 3 and 4). However, gene content is informative in that region suggesting that the species largely conform to the expected clustering even though the tree is not well supported (Figure 3). The difficulties are caused by a paucity of organizational changes that differentiate species at OriI - such as the inversion of three genes that sets apart the V. fisheri. Frequently, a change is unique to a sequenced strain and not shared by other members of its species. This can be extraordinarily disruptive of a distance estimate if the number of unique differences is large. In particular, at least three obvious saltations in the gene content introduce spikes of noise. In V. cholerae B33, an apparently mobile genetic region has imposed itself very close to the origin of replication. These 18 genes, almost as large as the region to be compared, interrupt an otherwise absolutely conserved region shared by the other Vibrio cholerae. A 9 gene region in Photobacterium sp. SKA34 contains several transposon and transposase genes. Similarly, 16 gene region in Vibrio splendidus MED222 interrupts an otherwise conserved region with a number of secretory system genes; it lacks apparent mobility elements which would explain its origin. Among the photobacteria, the flanking regions sometimes differ dramatically, as well, which disturbs the phylogeny with a very long branch, and the Vibrio cholerae appear to have inverted the entire region - but this would not impact a gene content analysis.

Bottom Line: Single copy genes from each chromosome (142 genes from chromosome I and 42 genes from chromosome II) were identified from 19 sequenced Vibrionales genomes and their phylogenetic comparison suggests consistent phylogenies for each chromosome.Additionally, study of the gene organization and phylogeny of the respective origins of replication confirmed the shared history.Thus, while elements within the chromosomes may have experienced significant genetic mobility, the backbones share a common history.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dept, of Civil and Environmental Engineering, 15 Vassar Street, Cambridge, MA 02139, USA. bckirkup@post.harvard.edu

ABSTRACT

Background: While most gamma proteobacteria have a single circular chromosome, Vibrionales have two circular chromosomes. Horizontal gene transfer is common among Vibrios, and in light of this genetic mobility, it is an open question to what extent the two chromosomes themselves share a common history since their formation.

Results: Single copy genes from each chromosome (142 genes from chromosome I and 42 genes from chromosome II) were identified from 19 sequenced Vibrionales genomes and their phylogenetic comparison suggests consistent phylogenies for each chromosome. Additionally, study of the gene organization and phylogeny of the respective origins of replication confirmed the shared history.

Conclusions: Thus, while elements within the chromosomes may have experienced significant genetic mobility, the backbones share a common history. This allows conclusions based on multilocus sequence analysis (MLSA) for one chromosome to be applied equally to both chromosomes.

Show MeSH