Limits...
Dynamics of genome rearrangement in bacterial populations.

Darling AE, Miklós I, Ragan MA - PLoS Genet. (2008)

Bottom Line: The inversion phylogenies agree with results suggested by SNP patterns.We found that all inversions are shorter than expected under a neutral model, whereas inversions acting within a single replichore are much shorter than expected.We also found evidence for a canonical configuration of the origin and terminus of replication.

View Article: PubMed Central - PubMed

Affiliation: ARC Center of Excellence in Bioinformatics, The University of Queensland, St. Lucia, Queensland, Australia. darling@cs.wisc.edu

ABSTRACT
Genome structure variation has profound impacts on phenotype in organisms ranging from microbes to humans, yet little is known about how natural selection acts on genome arrangement. Pathogenic bacteria such as Yersinia pestis, which causes bubonic and pneumonic plague, often exhibit a high degree of genomic rearrangement. The recent availability of several Yersinia genomes offers an unprecedented opportunity to study the evolution of genome structure and arrangement. We introduce a set of statistical methods to study patterns of rearrangement in circular chromosomes and apply them to the Yersinia. We constructed a multiple alignment of eight Yersinia genomes using Mauve software to identify 78 conserved segments that are internally free from genome rearrangement. Based on the alignment, we applied Bayesian statistical methods to infer the phylogenetic inversion history of Yersinia. The sampling of genome arrangement reconstructions contains seven parsimonious tree topologies, each having different histories of 79 inversions. Topologies with a greater number of inversions also exist, but were sampled less frequently. The inversion phylogenies agree with results suggested by SNP patterns. We then analyzed reconstructed inversion histories to identify patterns of rearrangement. We confirm an over-representation of "symmetric inversions"-inversions with endpoints that are equally distant from the origin of chromosomal replication. Ancestral genome arrangements demonstrate moderate preference for replichore balance in Yersinia. We found that all inversions are shorter than expected under a neutral model, whereas inversions acting within a single replichore are much shorter than expected. We also found evidence for a canonical configuration of the origin and terminus of replication. Finally, breakpoint reuse analysis reveals that inversions with endpoints proximal to the origin of DNA replication are nearly three times more frequent. Our findings represent the first characterization of genome arrangement evolution in a bacterial population evolving outside laboratory conditions. Insight into the process of genomic rearrangement may further the understanding of pathogen population dynamics and selection on the architecture of circular bacterial chromosomes.

Show MeSH

Related in: MedlinePlus

Episodes of imbalance in Yersinia.Left: The Bayesian posterior distribution of the number of imbalance episodes occurring entirely on branches of reconstructed inversion phylogenies, compared with permuted data. Right: Posterior distribution of the imbalance episode duration (in mutation events) observed on branches, compared with data permuted as described in the text. From the two plots we can conclude that transitions to imbalance are less frequent than expected under a  model, and that imbalance episodes last longer than expected under the  model.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2483231&req=5

pgen-1000128-g006: Episodes of imbalance in Yersinia.Left: The Bayesian posterior distribution of the number of imbalance episodes occurring entirely on branches of reconstructed inversion phylogenies, compared with permuted data. Right: Posterior distribution of the imbalance episode duration (in mutation events) observed on branches, compared with data permuted as described in the text. From the two plots we can conclude that transitions to imbalance are less frequent than expected under a model, and that imbalance episodes last longer than expected under the model.

Mentions: Our inference method does not estimate event times but only relative event ordering, thus we are unable to directly infer the actual amount of time ancestral genomes have spent in a balanced state. However, if we define a state of imbalance as a percentage deviation from perfect balance, say a 20% deviation, then we can quantify the number of imbalance episodes that the organisms have undergone. The posterior estimate of the number of imbalance episodes the eight Yersinia have undergone is 3.26 (σ = 1.82), not counting episodes which span a bifurcation event in the tree. The posterior distribution is shown at left in Figure 6. Similarly, we can define the duration of an imbalance episode as the number of mutation events (inversions) experienced before the chromosome returns to a balanced state. The length of imbalance episodes observed in our posterior sampling is shown at right in Figure 6.


Dynamics of genome rearrangement in bacterial populations.

Darling AE, Miklós I, Ragan MA - PLoS Genet. (2008)

Episodes of imbalance in Yersinia.Left: The Bayesian posterior distribution of the number of imbalance episodes occurring entirely on branches of reconstructed inversion phylogenies, compared with permuted data. Right: Posterior distribution of the imbalance episode duration (in mutation events) observed on branches, compared with data permuted as described in the text. From the two plots we can conclude that transitions to imbalance are less frequent than expected under a  model, and that imbalance episodes last longer than expected under the  model.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2483231&req=5

pgen-1000128-g006: Episodes of imbalance in Yersinia.Left: The Bayesian posterior distribution of the number of imbalance episodes occurring entirely on branches of reconstructed inversion phylogenies, compared with permuted data. Right: Posterior distribution of the imbalance episode duration (in mutation events) observed on branches, compared with data permuted as described in the text. From the two plots we can conclude that transitions to imbalance are less frequent than expected under a model, and that imbalance episodes last longer than expected under the model.
Mentions: Our inference method does not estimate event times but only relative event ordering, thus we are unable to directly infer the actual amount of time ancestral genomes have spent in a balanced state. However, if we define a state of imbalance as a percentage deviation from perfect balance, say a 20% deviation, then we can quantify the number of imbalance episodes that the organisms have undergone. The posterior estimate of the number of imbalance episodes the eight Yersinia have undergone is 3.26 (σ = 1.82), not counting episodes which span a bifurcation event in the tree. The posterior distribution is shown at left in Figure 6. Similarly, we can define the duration of an imbalance episode as the number of mutation events (inversions) experienced before the chromosome returns to a balanced state. The length of imbalance episodes observed in our posterior sampling is shown at right in Figure 6.

Bottom Line: The inversion phylogenies agree with results suggested by SNP patterns.We found that all inversions are shorter than expected under a neutral model, whereas inversions acting within a single replichore are much shorter than expected.We also found evidence for a canonical configuration of the origin and terminus of replication.

View Article: PubMed Central - PubMed

Affiliation: ARC Center of Excellence in Bioinformatics, The University of Queensland, St. Lucia, Queensland, Australia. darling@cs.wisc.edu

ABSTRACT
Genome structure variation has profound impacts on phenotype in organisms ranging from microbes to humans, yet little is known about how natural selection acts on genome arrangement. Pathogenic bacteria such as Yersinia pestis, which causes bubonic and pneumonic plague, often exhibit a high degree of genomic rearrangement. The recent availability of several Yersinia genomes offers an unprecedented opportunity to study the evolution of genome structure and arrangement. We introduce a set of statistical methods to study patterns of rearrangement in circular chromosomes and apply them to the Yersinia. We constructed a multiple alignment of eight Yersinia genomes using Mauve software to identify 78 conserved segments that are internally free from genome rearrangement. Based on the alignment, we applied Bayesian statistical methods to infer the phylogenetic inversion history of Yersinia. The sampling of genome arrangement reconstructions contains seven parsimonious tree topologies, each having different histories of 79 inversions. Topologies with a greater number of inversions also exist, but were sampled less frequently. The inversion phylogenies agree with results suggested by SNP patterns. We then analyzed reconstructed inversion histories to identify patterns of rearrangement. We confirm an over-representation of "symmetric inversions"-inversions with endpoints that are equally distant from the origin of chromosomal replication. Ancestral genome arrangements demonstrate moderate preference for replichore balance in Yersinia. We found that all inversions are shorter than expected under a neutral model, whereas inversions acting within a single replichore are much shorter than expected. We also found evidence for a canonical configuration of the origin and terminus of replication. Finally, breakpoint reuse analysis reveals that inversions with endpoints proximal to the origin of DNA replication are nearly three times more frequent. Our findings represent the first characterization of genome arrangement evolution in a bacterial population evolving outside laboratory conditions. Insight into the process of genomic rearrangement may further the understanding of pathogen population dynamics and selection on the architecture of circular bacterial chromosomes.

Show MeSH
Related in: MedlinePlus