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.2013 Mar 26;4(2):e00604-12.
doi: 10.1128/mBio.00604-12.

Comparative analysis of Chlamydia psittaci genomes reveals the recent emergence of a pathogenic lineage with a broad host range

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Comparative analysis of Chlamydia psittaci genomes reveals the recent emergence of a pathogenic lineage with a broad host range

Timothy D Read et al. mBio..

Abstract

Chlamydia psittaci is an obligate intracellular bacterium. Interest in Chlamydia stems from its high degree of virulence as an intestinal and pulmonary pathogen across a broad range of animals, including humans. C. psittaci human pulmonary infections, referred to as psittacosis, can be life-threatening, which is why the organism was developed as a bioweapon in the 20th century and is listed as a CDC biothreat agent. One remarkable recent result from comparative genomics is the finding of frequent homologous recombination across the genome of the sexually transmitted and trachoma pathogen Chlamydia trachomatis. We sought to determine if similar evolutionary dynamics occurred in C. psittaci. We analyzed 20 C. psittaci genomes from diverse strains representing the nine known serotypes of the organism as well as infections in a range of birds and mammals, including humans. Genome annotation revealed a core genome in all strains of 911 genes. Our analyses showed that C. psittaci has a history of frequently switching hosts and undergoing recombination more often than C. trachomatis. Evolutionary history reconstructions showed genome-wide homologous recombination and evidence of whole-plasmid exchange. Tracking the origins of recombinant segments revealed that some strains have imported DNA from as-yet-unsampled or -unsequenced C. psittaci lineages or other Chlamydiaceae species. Three ancestral populations of C. psittaci were predicted, explaining the current population structure. Molecular clock analysis found that certain strains are part of a clonal epidemic expansion likely introduced into North America by South American bird traders, suggesting that psittacosis is a recently emerged disease originating in New World parrots.

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Figures

FIG 1
FIG 1
Whole-genome phylogeny ofC. psittaci. The tree was constructed using a neighbor-joining algorithm based on whole-genome alignment (see Materials and Methods). The 6BC Clade 1 is highlighted in blue, and Clades 2 and 3 are in green and red, respectively. All branches were supported by 100% confidence in 100 bootstrap samplings except for some branches internal to the 6BC Clade (not shown) and the Borg/NJ1/FalTex branch. The scale is in substitutions per position.
FIG 2
FIG 2
Comparison of the plasticity zones (PZs) ofC. psittaci 6BC and RTH andC. abortus S26/3. The structure in the center shows the order of genes in the PZ of 6BC, with the numbers referring to the locus tag prefix (see RefSeq accession NC_017287.1). Some small genes (<150 nucleotides) were omitted in order to make the diagram less complex. The genes are color coded by function and matched to best hits in the other genomes. Genes with diagonal slashes are predicted to have loss-of-function frameshifts.
FIG 3
FIG 3
Results of the ClonalFrame analysis on an alignment of the 20C. psittaci genomes. The inferred clonal genealogy is shown on the left. Each branch of the tree corresponds to a row of the heat map, which is horizontally aligned with it according to the core MAUVE whole-genome alignment. Each row of the heat map shows the posterior probability of recombination estimated by ClonalFrame on the corresponding branch (y axis) and along the positions of the alignment (x axis).
FIG 4
FIG 4
BLAST analysis of origins of recombinant fragments. Distribution of the best BLASTN hits of the putative recombinant segments identified by ClonalFrame and nonrecombinant regions extracted randomly (within the range of the size of recombinant segments) categorized based on 4 ranges of percent identity. For each of the clades/strains, both the recombinant segments and the nonrecombinant segments were searched against a BLAST database containing all theC. psittaci genomes minus the strain/clade that was affected by the import using BLASTN. Clade 2 (FalTex, Borg, and NJ1) contained a minimal number of recombinant segments, which were shorter to perform, and, therefore, BLASTN analysis was not included here.
FIG 5
FIG 5
Bar plot representing the result from the STRUCTURE linkage model. Each vertical line represents one of the 20C. psittaci strains. They axis shows the proportion of ancestry from each of the three ancestral populations. The tree at the top represents a complete linkage clustering of the strains based on their proportions of ancestry from each population and are represented by different groups as noted. The lettering of each strain is color coded to identify clades as in Fig. 1.
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References

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