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Chromosomal rearrangements formed by rrn recombination do not improve replichore balance in host-specific Salmonella enterica serovars.

Matthews TD, Edwards R, Maloy S - PLoS ONE (2010)

Bottom Line: Only 48 out of 1,440 possible arrangement types were identified in 212 host-specific strains.While the replichores of most naturally-occurring arrangement types were well-balanced, most theoretical arrangement types had imbalanced replichores.Furthermore, the most common types of rearrangements did not change replichore balance.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Center for Microbial Sciences, San Diego State University, San Diego, California, United States of America.

ABSTRACT

Background: Most of the ∼2,600 serovars of Salmonella enterica have a broad host range as well as a conserved gene order. In contrast, some Salmonella serovars are host-specific and frequently exhibit large chromosomal rearrangements from recombination between rrn operons. One hypothesis explaining these rearrangements suggests that replichore imbalance introduced from horizontal transfer of pathogenicity islands and prophages drives chromosomal rearrangements in an attempt to improve balance.

Methodology/principal findings: This hypothesis was directly tested by comparing the naturally-occurring chromosomal arrangement types to the theoretically possible arrangement types, and estimating their replichore balance using a calculator. In addition to previously characterized strains belonging to host-specific serovars, the arrangement types of 22 serovar Gallinarum strains was also determined. Only 48 out of 1,440 possible arrangement types were identified in 212 host-specific strains. While the replichores of most naturally-occurring arrangement types were well-balanced, most theoretical arrangement types had imbalanced replichores. Furthermore, the most common types of rearrangements did not change replichore balance.

Conclusions/significance: The results did not support the hypothesis that replichore imbalance causes these rearrangements, and suggest that the rearrangements could be explained by aspects of a host-specific lifestyle.

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Related in: MedlinePlus

The conserved rrn arrangement type 1234567 found in the broad host range serovars of Salmonella enterica.The seven rrn operons are lettered while the regions in between the operons are numbered. The origin of replication is indicated by a green circle and the terminus region is highlighted in red. Replichores are the chromosomal halves between the origin and terminus of replication.
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pone-0013503-g001: The conserved rrn arrangement type 1234567 found in the broad host range serovars of Salmonella enterica.The seven rrn operons are lettered while the regions in between the operons are numbered. The origin of replication is indicated by a green circle and the terminus region is highlighted in red. Replichores are the chromosomal halves between the origin and terminus of replication.

Mentions: Another aspect of chromosomal organization that may limit plasticity is replichore balance [26], [27]. In most sequenced bacterial chromosomes, the replichores, opposite sides of the chromosome between the origin of DNA replication and the terminus, are equal in length with the origin 180° around the chromosome from the terminus (Figure 1) [28], [29]. When replichores are of equal length, DNA replication is balanced. Many types of chromosomal rearrangements can make one replichore longer than the other, altering the amount of time required to replicate each replichore. Even though strains having imbalanced replichores are rare because unbalanced replication is thought to affect fitness [22], [26], [30], replichore balance can still vary within the same species [4], [26], [27].


Chromosomal rearrangements formed by rrn recombination do not improve replichore balance in host-specific Salmonella enterica serovars.

Matthews TD, Edwards R, Maloy S - PLoS ONE (2010)

The conserved rrn arrangement type 1234567 found in the broad host range serovars of Salmonella enterica.The seven rrn operons are lettered while the regions in between the operons are numbered. The origin of replication is indicated by a green circle and the terminus region is highlighted in red. Replichores are the chromosomal halves between the origin and terminus of replication.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2957434&req=5

pone-0013503-g001: The conserved rrn arrangement type 1234567 found in the broad host range serovars of Salmonella enterica.The seven rrn operons are lettered while the regions in between the operons are numbered. The origin of replication is indicated by a green circle and the terminus region is highlighted in red. Replichores are the chromosomal halves between the origin and terminus of replication.
Mentions: Another aspect of chromosomal organization that may limit plasticity is replichore balance [26], [27]. In most sequenced bacterial chromosomes, the replichores, opposite sides of the chromosome between the origin of DNA replication and the terminus, are equal in length with the origin 180° around the chromosome from the terminus (Figure 1) [28], [29]. When replichores are of equal length, DNA replication is balanced. Many types of chromosomal rearrangements can make one replichore longer than the other, altering the amount of time required to replicate each replichore. Even though strains having imbalanced replichores are rare because unbalanced replication is thought to affect fitness [22], [26], [30], replichore balance can still vary within the same species [4], [26], [27].

Bottom Line: Only 48 out of 1,440 possible arrangement types were identified in 212 host-specific strains.While the replichores of most naturally-occurring arrangement types were well-balanced, most theoretical arrangement types had imbalanced replichores.Furthermore, the most common types of rearrangements did not change replichore balance.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Center for Microbial Sciences, San Diego State University, San Diego, California, United States of America.

ABSTRACT

Background: Most of the ∼2,600 serovars of Salmonella enterica have a broad host range as well as a conserved gene order. In contrast, some Salmonella serovars are host-specific and frequently exhibit large chromosomal rearrangements from recombination between rrn operons. One hypothesis explaining these rearrangements suggests that replichore imbalance introduced from horizontal transfer of pathogenicity islands and prophages drives chromosomal rearrangements in an attempt to improve balance.

Methodology/principal findings: This hypothesis was directly tested by comparing the naturally-occurring chromosomal arrangement types to the theoretically possible arrangement types, and estimating their replichore balance using a calculator. In addition to previously characterized strains belonging to host-specific serovars, the arrangement types of 22 serovar Gallinarum strains was also determined. Only 48 out of 1,440 possible arrangement types were identified in 212 host-specific strains. While the replichores of most naturally-occurring arrangement types were well-balanced, most theoretical arrangement types had imbalanced replichores. Furthermore, the most common types of rearrangements did not change replichore balance.

Conclusions/significance: The results did not support the hypothesis that replichore imbalance causes these rearrangements, and suggest that the rearrangements could be explained by aspects of a host-specific lifestyle.

Show MeSH
Related in: MedlinePlus