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Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts.

ABSTRACT: Various bacteria live exclusively within arthropod cells and collectively act as an important driver of arthropod evolutionary ecology. Whereas rampant intra-generic DNA transfers were recently shown to have a pivotal role in the evolution of the most common of these endosymbionts, Wolbachia, the present study show that inter-generic DNA transfers also commonly take place, constituting a potent source of rapid genomic change. Bioinformatic, molecular and phylogenetic data provide evidence that a selfish genetic element, the insertion sequence ISRpe1, is widespread in the Wolbachia, Cardinium and Rickettsia endosymbionts and experiences recent (and likely ongoing) transfers over long evolutionary distances. Although many ISRpe1 copies were clearly expanding and leading to rapid endosymbiont diversification, degraded copies are also frequently found, constituting an unusual genomic fossil record suggestive of ancient ISRpe1 expansions. Overall, the present data highlight how ecological connections within the arthropod intracellular environment facilitate lateral DNA transfers between distantly related bacterial lineages.

SUBMITTER: Duron O

PROVIDER: S-EPMC3807263 | biostudies-literature | 2013 Oct

REPOSITORIES: biostudies-literature

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Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts.

Duron O O

Heredity 20130612 4

Various bacteria live exclusively within arthropod cells and collectively act as an important driver of arthropod evolutionary ecology. Whereas rampant intra-generic DNA transfers were recently shown to have a pivotal role in the evolution of the most common of these endosymbionts, Wolbachia, the present study show that inter-generic DNA transfers also commonly take place, constituting a potent source of rapid genomic change. Bioinformatic, molecular and phylogenetic data provide evidence that a ...[more]

PMID: 23759724

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Project description:The bacterial endosymbiont Wolbachia interacts with different invertebrate hosts, engaging in diverse symbiotic relationships. Wolbachia is often a reproductive parasite in arthropods, but an obligate mutualist in filarial nematodes. Wolbachia was recently discovered in plant-parasitic nematodes, and, is thus far known in just two genera Pratylenchus and Radopholus, yet the symbiont's function remains unknown. The occurrence of Wolbachia in these economically important plant pests offers an unexplored biocontrol strategy. However, development of Wolbachia-based biocontrol requires an improved understanding of symbiont-host functional interactions and the symbiont's prevalence among nematode field populations. This study used a molecular-genetic approach to assess the prevalence of a Wolbachia lineage (wPpe) in 32 field populations of Pratylenchus penetrans. Populations were examined from eight different plant species in Washington, Oregon, and California. Nematodes were also screened for the endosymbiotic bacterium Cardinium (cPpe) that was recently shown to co-infect P. penetrans. Results identified wPpe in 9/32 and cPpe in 1/32 of P. penetrans field populations analyzed. No co-infection was observed in field populations. Wolbachia was detected in nematodes from 4/8 plant-hosts examined (raspberry, strawberry, clover, and lily), and in all three states surveyed. Cardinium was detected in nematodes from mint in Washington. In the wPpe-infected P. penetrans populations collected from raspberry, the prevalence of wPpe infection ranged from 11 to 58%. This pattern is unlike that in filarial nematodes where Wolbachia is an obligate mutualist and occurs in 100% of the host. Further analysis of wPpe-infected populations revealed female-skewed sex ratios (up to 96%), with the degree of skew positively correlating with wPpe prevalence. Uninfected nematode populations had approximately equal numbers of males and females. Comparisons of 54 wPpe 16S ribosomal RNA sequences revealed high similarity across the geographic isolates, with 45 of 54 isolates being identical at this locus. The complete absence of wPpe among some populations and low prevalence in others suggest that this endosymbiont is not an obligate mutualist of P. penetrans. The observed sex ratio bias in wPpe-infected nematode populations is similar to that observed in arthropods where Wolbachia acts as a reproductive manipulator, raising the question of a similar role in plant-parasitic nematodes.

Project description:BACKGROUND: Wolbachia and Cardinium are endosymbiotic bacteria infecting many arthropods and manipulating host reproduction. Although these bacteria are maternally transmitted, incongruencies between phylogenies of host and parasite suggest an additional role for occasional horizontal transmission. Consistent with this view is the strong evidence for recombination in Wolbachia, although it is less clear to what extent recombination drives diversification within single host species and genera. Furthermore, little is known concerning the population structures of other insect endosymbionts which co-infect with Wolbachia, such as Cardinium. Here, we explore Wolbachia and Cardinium strain diversity within nine spider mite species (Tetranychidae) from 38 populations, and quantify the contribution of recombination compared to point mutation in generating Wolbachia diversity. RESULTS: We found a high level of genetic diversity for Wolbachia, with 36 unique strains detected (64 investigated mite individuals). Sequence data from four Wolbachia genes suggest that new alleles are 7.5 to 11 times more likely to be generated by recombination than point mutation. Consistent with previous reports on more diverse host samples, our data did not reveal evidence for co-evolution of Wolbachia with its host. Cardinium was less frequently found in the mites, but also showed a high level of diversity, with eight unique strains detected in 15 individuals on the basis of only two genes. A lack of congruence among host and Cardinium phylogenies was observed. CONCLUSIONS: We found a high rate of recombination for Wolbachia strains obtained from host species of the spider mite family Tetranychidae, comparable to rates found for horizontally transmitted bacteria. This suggests frequent horizontal transmission of Wolbachia and/or frequent horizontal transfer of single genes. Our findings strengthens earlier reports of recombination for Wolbachia, and shows that high recombination rates are also present on strains from a restrictive host range. Cardinium was found co-infecting several spider mite species, and phylogenetic comparisons suggest also horizontal transmission of Cardinium among hosts.

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

Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts.

Publications

Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts.

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