Evolution and diversity of Rickettsia bacteria

Abstract

Background: Rickettsia are intracellular symbionts of eukaryotes that are best known for infecting and causing serious diseases in humans and other mammals. All known vertebrate-associated Rickettsia are vectored by arthropods as part of their life-cycle, and many other Rickettsia are found exclusively in arthropods with no known secondary host. However, little is known about the biology of these latter strains. Here, we have identified 20 new strains of Rickettsia from arthropods, and constructed a multi-gene phylogeny of the entire genus which includes these new strains.

Results: We show that Rickettsia are primarily arthropod-associated bacteria, and identify several novel groups within the genus. Rickettsia do not co-speciate with their hosts but host shifts most often occur between related arthropods. Rickettsia have evolved adaptations including transmission through vertebrates and killing males in some arthropod hosts. We uncovered one case of horizontal gene transfer among Rickettsia, where a strain is a chimera from two distantly related groups, but multi-gene analysis indicates that different parts of the genome tend to share the same phylogeny.

Conclusion: Approximately 150 million years ago, Rickettsia split into two main clades, one of which primarily infects arthropods, and the other infects a diverse range of protists, other eukaryotes and arthropods. There was then a rapid radiation about 50 million years ago, which coincided with the evolution of life history adaptations in a few branches of the phylogeny. Even though Rickettsia are thought to be primarily transmitted vertically, host associations are short lived with frequent switching to new host lineages. Recombination throughout the genus is generally uncommon, although there is evidence of horizontal gene transfer. A better understanding of the evolution of Rickettsia will help in the future to elucidate the mechanisms of pathogenicity, transmission and virulence.

Figure 1

Phylogeny of Rickettsia. The name of the host prefixed by (s) is given where the bacterium does not have a species name, as well as names for each Rickettsia group, life history and host order. (a) Bayesian phylogeny using concatenated sequences of atpA, coxA, gltA, 16S. Posterior support for each node is shown. (b) Maximum likelihood phylogeny based on complete sequences of atpA, coxA and gltA. Bootstrap support is given as a percentage above the node, and posterior support from a Bayesian tree is given as a decimal below the node. ^aPreviously characterised groups. ^bOnly circumstantial evidence connects the trait to the strain.

Figure 2

Relationships and approximate dates of divergence of the major clades within the order Rickettsiales. The 16S rDNA phylogeny was reconstructed using one member of each of the groups shown with a molecular clock enforced (enforcing the clock did not reduce the likelihood of the tree: likelihood ratio test lnL = 13.84, df = 12 p = 0.311).

Figure 3

Sequence alignment and hybridisation network showing the symbiont of Coccidula rufa to be a recombinant. (a) Alignment of concatenated genes atpA, coxA, gltA, 16S showing just polymorphic sites. Nucleotides that are identical to the C. rufa sequence are shown as a dot. The (s)C. rufa sequence of atpA and coxA (shaded) are most similar to (s)Elateridae in the bellii group, while the gltA and 16S sequences (unshaded) are most similar to (s)Pediobius rotundus in the transitional group. (b) A hybridisation network of the concatenated sequences of atpA, coxA, gltA and 16S. A neighbour-net split network was generated and splits were then filtered by weight to include only the (s)C. rufa split. A hybridisation network was then performed on the split network to provide an explicit example of descent from the two different groups.