Comparative Analysis of Chlamydia psittaci Genomes Reveals the Recent Emergence of a Pathogenic Lineage with a Broad Host Range

Chlamydia psittaci is an obligate intracellular bacterium. Interest inChlamydia 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 pathogenChlamydia trachomatis . We sought to determine if similar evolutionary dynamics occurred inC. psittaci . We analyzed 20C. 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 thatC. psittaci has a history of frequently switching hosts and undergoing recombination more often thanC. 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 -unsequencedC. psittaci lineages or otherChlamydiaceae species. Three ancestral populations ofC. 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.IMPORTANCE Chlamydia psittaci is classified as a CDC biothreat agent based on its association with life-threatening lung disease, termed psittacosis, in humans. Because of the recent remarkable findings of frequent recombination across the genome of the human sexually transmitted and ocular trachoma pathogenChlamydia trachomatis , we sought to determine if similar evolutionary dynamics occur inC. psittaci . TwentyC. psittaci genomes were analyzed from diverse strains that may play a pathogenic role in human disease. Evolution of the strains revealed genome-wide recombination occurring at a higher rate than forC. trachomatis . Certain strains were discovered to be part of a recent epidemic clonal expansion originating in South America. These strains may have been introduced into the United States from South American bird traders, suggesting that psittacosis is a recently emerged disease originating in New World parrots. Our analyses indicate thatC. psittaci strains have a history of frequently switching hosts and undergoing recombination.