Genome Sequence of Rickettsia bellii Illuminates the Role of Amoebae in Gene Exchanges between Intracellular Pathogens

Top Cited Papers
Open Access
Publisher Website
Google Scholar
Abstract
The recently sequenced Rickettsia felis genome revealed an unexpected plasmid carrying several genes usually associated with DNA transfer, suggesting that ancestral rickettsiae might have been endowed with a conjugation apparatus. Here we present the genome sequence of Rickettsia bellii, the earliest diverging species of known rickettsiae. The 1,552,076 base pair–long chromosome does not exhibit the colinearity observed between other rickettsia genomes, and encodes a complete set of putative conjugal DNA transfer genes most similar to homologues found in Protochlamydia amoebophila UWE25, an obligate symbiont of amoebae. The genome exhibits many other genes highly similar to homologues in intracellular bacteria of amoebae. We sought and observed sex pili-like cell surface appendages for R. bellii. We also found that R. bellii very efficiently multiplies in the nucleus of eukaryotic cells and survives in the phagocytic amoeba, Acanthamoeba polyphaga. These results suggest that amoeba-like ancestral protozoa could have served as a genetic “melting pot” where the ancestors of rickettsiae and other bacteria promiscuously exchanged genes, eventually leading to their adaptation to the intracellular lifestyle within eukaryotic cells. Obligate intracellular pathogens, by their isolated way of life, are thought to have little opportunity to exchange DNA with other microbes, making their genome relatively immune to horizontal gene transfer. Rickettsia bellii is the earliest diverging species of Rickettsia, a group of obligate intracellular bacteria causing human diseases such as epidemic typhus. Sequencing and computer analysis of its genome now provides evidence that many genes were transferred between the ancestors of Rickettsia and other microbes living inside amoebae, including the human pathogen Legionella pneumophila and the chlamydia-related symbiont Protochlamydia amoebophila. Remarkably, R. bellii exhibits a complete set of predicted genes for conjugative DNA transfer. Microscopic analyses confirmed this prediction by revealing bacterial mating through sex pili-like surface appendages. Furthermore, the authors demonstrate that R. bellii can survive in an amoeba for a long period of time. Taken together, these results suggest that amoeba-like ancestral protozoa acted as a “breeding ground” for different bacteria, promoting acquisition of the gene repertoire required to infect the cells of higher eukaryotes.