The relationship between humans and their obligate parasite, Streptococcus mutans, is important for elucidating why different strains have different pathogenic potentials. Some strains of S. mutans also harbor a parasitic plasmid of unknown function. Objective: According, we examined the chromosomal frame of plasmid-containing strains of S. mutans and compared the phylogenetic relationships among parasites with the racial/geographic history of their human host. Methods: Using information from chromosomal DNA fingerprints (CDF), a hypervariable region (HVR) of a 5.6-kb plasmid, the ribosomal DNA intergenic spacer region (IGSR), serotypes, and mutacin genotypes, we made inferences as to phylogeny. Results: The CDF of S. mutans from unrelated human hosts were unique, except those from Caucasians, which were essentially identical. Phylogenies using sequences from the IGSR, with or without the serotype and mutacin characters, showed a clearly distinguished Asian clade. Also, a continuous association with mutacin II could be reconstructed for an evolutionary lineage, but association with serotype e was evolutionarily homoplastic. Genetic diversity among plasmid-containing strains was twice as great as that among the plasmid-free strains. Not unexpectedly, DNA sequences from the HVR of the plasmid produced a well-resolved phylogeny that differed from the chromosomal phylogeny, suggesting that horizontal transfer of the plasmid has occurred multiple times. The plasmid phylogeny was more congruent with serotype e than with mutacin II evolution, suggesting a possible functional correlation. Conclusion: The evolutionary history of this three-tiered relationship between human, bacterium and plasmid, shows both coevolution and independent evolution. This work supported by NIH/NIDCR grants DE13937 and DE011147.

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