Background: The genomes of pathogens are thought to have evolved under selective pressure provided by the host in a coevolutionary arms race (the 'Red Queen's Hypothesis'). Traditionally, adaptation by pathogens is thought to rely not on whole chromosome dynamics but on gain/loss of specific genes, yielding differential abilities to infect distinct tissues. Thus, it is not known whether distinct host organs differently shape the genome of the same pathogen. We tested this hypothesis using Chlamydia trachomatis as model species, looking at 15 serovars that infect different organs: eyes, genitalia and lymph nodes.
Results: We analyzed over 51,000 base pairs from all serovars using various phylogenetic approaches and a non-phylogenetic indel-based algorithm to study the evolution of individual and concatenated loci. This survey comprised about 33% of all single nucleotide polymorphisms in C. trachomatis chromosomes. We present a model in which genome evolution indeed correlates with the cell type (epithelial versus lymph cells) and organ (eyes versus genitalia) that a serovar infects, illustrating an adaptation to physiologically distinct niches, and discarding genetic drift as the dominant evolutionary driving force. We show that radiation of serovars occurred primarily by accumulation of single nucleotide polymorphisms in intergenomic regions, housekeeping genes, and genes encoding hypothetical and cell envelope proteins. Furthermore, serovar evolution also correlates with ecological success, as the two most successful serovars showed a parallel evolution.
Conclusion: We identified a single nucleotide polymorphism-based tissue-specific arms race for strains in the same species, reflecting global chromosomal dynamics. Studying such tissue-specific arms race scenarios is crucial for understanding pathogen-host interactions during the course of infectious diseases, in order to dissect pathogen biology and develop preventive and therapeutic strategies.