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Evolution and diversity of Rickettsia bacteria.

Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM - BMC Biol. (2009)

Bottom Line: 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.Rickettsia do not co-speciate with their hosts but host shifts most often occur between related arthropods.Recombination throughout the genus is generally uncommon, although there is evidence of horizontal gene transfer.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3JT, UK. lucy.weinert@ed.ac.uk

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.

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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.
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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.

Mentions: Recombination events complicate the inference of species trees, and so it is important to investigate the extent of recombination in the Rickettsia genus. We found one clear instance of recent recombination between different Rickettsia groups (this taxon was excluded from the analyses above). In the phylogenetic trees of the four individual genes (Additional file 2, Phylogenetic trees of each of the individual genes used in the study), the symbiont of the ladybird Coccidula rufa (sC. rufa) appears in the transitional group on the 16S and gltA trees, and in the bellii group on the atpA and coxA trees. An alignment of the polymorphic sites and a hybridisation network indicates that sC. rufa is a chimera of sequences from these two groups (Figure 3). To verify that the recombination pattern for sC. rufa was not the result of contamination, this result was confirmed by sequencing three strains from different individuals of C. rufa. This appears to be the only case of recombination between the four genes because when sC. rufa is excluded from analyses, there is little evidence of topological differences between the datasets (see SH tests above).


Evolution and diversity of Rickettsia bacteria.

Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM - BMC Biol. (2009)

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.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2662801&req=5

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.
Mentions: Recombination events complicate the inference of species trees, and so it is important to investigate the extent of recombination in the Rickettsia genus. We found one clear instance of recent recombination between different Rickettsia groups (this taxon was excluded from the analyses above). In the phylogenetic trees of the four individual genes (Additional file 2, Phylogenetic trees of each of the individual genes used in the study), the symbiont of the ladybird Coccidula rufa (sC. rufa) appears in the transitional group on the 16S and gltA trees, and in the bellii group on the atpA and coxA trees. An alignment of the polymorphic sites and a hybridisation network indicates that sC. rufa is a chimera of sequences from these two groups (Figure 3). To verify that the recombination pattern for sC. rufa was not the result of contamination, this result was confirmed by sequencing three strains from different individuals of C. rufa. This appears to be the only case of recombination between the four genes because when sC. rufa is excluded from analyses, there is little evidence of topological differences between the datasets (see SH tests above).

Bottom Line: 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.Rickettsia do not co-speciate with their hosts but host shifts most often occur between related arthropods.Recombination throughout the genus is generally uncommon, although there is evidence of horizontal gene transfer.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3JT, UK. lucy.weinert@ed.ac.uk

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.

Show MeSH
Related in: MedlinePlus