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Comparative genomics of Wolbachia and the bacterial species concept.

ABSTRACT: The importance of host-specialization to speciation processes in obligate host-associated bacteria is well known, as is also the ability of recombination to generate cohesion in bacterial populations. However, whether divergent strains of highly recombining intracellular bacteria, such as Wolbachia, can maintain their genetic distinctness when infecting the same host is not known. We first developed a protocol for the genome sequencing of uncultivable endosymbionts. Using this method, we have sequenced the complete genomes of the Wolbachia strains wHa and wNo, which occur as natural double infections in Drosophila simulans populations on the Seychelles and in New Caledonia. Taxonomically, wHa belong to supergroup A and wNo to supergroup B. A comparative genomics study including additional strains supported the supergroup classification scheme and revealed 24 and 33 group-specific genes, putatively involved in host-adaptation processes. Recombination frequencies were high for strains of the same supergroup despite different host-preference patterns, leading to genomic cohesion. The inferred recombination fragments for strains of different supergroups were of short sizes, and the genomes of the co-infecting Wolbachia strains wHa and wNo were not more similar to each other and did not share more genes than other A- and B-group strains that infect different hosts. We conclude that Wolbachia strains of supergroup A and B represent genetically distinct clades, and that strains of different supergroups can co-exist in the same arthropod host without converging into the same species. This suggests that the supergroups are irreversibly separated and that barriers other than host-specialization are able to maintain distinct clades in recombining endosymbiont populations. Acquiring a good knowledge of the barriers to genetic exchange in Wolbachia will advance our understanding of how endosymbiont communities are constructed from vertically and horizontally transmitted genes.

SUBMITTER: Ellegaard KM

PROVIDER: S-EPMC3616963 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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Comparative genomics of Wolbachia and the bacterial species concept.

Ellegaard Kirsten Maren KM Klasson Lisa L Näslund Kristina K Bourtzis Kostas K Andersson Siv G E SG

PLoS genetics 20130404 4

The importance of host-specialization to speciation processes in obligate host-associated bacteria is well known, as is also the ability of recombination to generate cohesion in bacterial populations. However, whether divergent strains of highly recombining intracellular bacteria, such as Wolbachia, can maintain their genetic distinctness when infecting the same host is not known. We first developed a protocol for the genome sequencing of uncultivable endosymbionts. Using this method, we have se ...[more]

PMID: 23593012

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Project description:Wolbachia pipientis are obligate intracellular bacteria commonly found in many arthropods. They can induce various reproductive alterations in hosts, including cytoplasmic incompatibility, male-killing, feminization, and parthenogenetic development, and can provide host protection against some viruses and other pathogens. Wolbachia differ from many other primary endosymbionts in arthropods because they undergo frequent horizontal transmission between hosts and are well known for an abundance of mobile elements and relatively high recombination rates. Here, we compare the genomes of two closely related Wolbachia (with 0.57% genome-wide synonymous divergence) that differ in their reproductive effects on hosts. wVitA induces a sperm-egg incompatibility (also known as cytoplasmic incompatibility) in the parasitoid insect Nasonia vitripennis, whereas wUni causes parthenogenetic development in a different parasitoid, Muscidifurax uniraptor Although these bacteria are closely related, the genomic comparison reveals rampant rearrangements, protein truncations (particularly in proteins predicted to be secreted), and elevated substitution rates. These changes occur predominantly in the wUni lineage, and may be due in part to adaptations by wUni to a new host environment, or its phenotypic shift to parthenogenesis induction. However, we conclude that the approximately 8-fold elevated synonymous substitution rate in wUni is due to a either an elevated mutation rate or a greater number of generations per year in wUni, which occurs in semitropical host species. We identify a set of genes whose loss or pseudogenization in the wUni lineage implicates them in the phenotypic shift from cytoplasmic incompatibility to parthenogenesis induction. Finally, comparison of these closely related strains allows us to determine the fine-scale mutation patterns in Wolbachia Although Wolbachia are AT rich, mutation probabilities estimated from 4-fold degenerate sites are not AT biased, and predict an equilibrium AT content much less biased than observed (57-50% AT predicted vs. 76% current content at degenerate sites genome wide). The contrast suggests selection for increased AT content within Wolbachia genomes.

Project description:Wolbachia and Cardinium are among the most important and widespread of all endosymbionts, occurring in nematodes and more than half of insect and arachnid species, sometimes as coinfections. These symbionts are of significant interest as potential biocontrol agents due to their abilities to cause major effects on host biology and reproduction through cytoplasmic incompatibility, sex ratio distortion, or obligate mutualism. The ecological and metabolic effects of coinfections are not well understood. This study examined a Wolbachia-Cardinium coinfection in the plant-parasitic nematode (PPN), Pratylenchus penetrans, producing the first detailed study of such a coinfection using fluorescence in situ hybridization (FISH), polymerase chain reaction (PCR), and comparative genomic analysis. Results from FISH and single-nematode PCR showed 123/127 individuals in a focal population carried Cardinium (denoted strain cPpe), and 48% were coinfected with Wolbachia strain wPpe. Both endosymbionts showed dispersed tissue distribution with highest densities in the anterior intestinal walls and gonads. Phylogenomic analyses confirmed an early place of cPpe and long distance from a sister strain in another PPN, Heterodera glycines, supporting a long history of both Cardinium and Wolbachia in PPNs. The genome of cPpe was 1.36 Mbp with 35.8% GC content, 1,131 predicted genes, 41% having no known function, and missing biotin and lipoate synthetic capacity and a plasmid present in other strains, despite having a slightly larger genome compared to other sequenced Cardinium. The larger genome revealed expansions of gene families likely involved in host-cellular interactions. More than 2% of the genes of cPpe and wPpe were identified as candidate horizontally transferred genes, with some of these from eukaryotes, including nematodes. A model of the possible Wolbachia-Cardinium interaction is proposed with possible complementation in function for pathways such as methionine and fatty acid biosynthesis and biotin transport.

Dataset Information

Comparative genomics of Wolbachia and the bacterial species concept.

Publications

Comparative genomics of Wolbachia and the bacterial species concept.

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