Regulation of Wolbachia ankyrin domain encoding genes in Drosophila gonads

Papafotiou, Georgios; Oehler, Stefan; Savakis, Charalambos; Bourtzis, Kostas

doi:10.1016/j.resmic.2011.06.012

Cited by 28 publications

(26 citation statements)

References 55 publications

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“…In contrast to the observations for w Pip [22,23], expression pattern of pk2b2 suggests that this allele is not involved in CI in isopods. In two recent studies, it has been shown that expression of pk1 and pk2 genes from w Mel was not correlated with the CI phenotype in D. melanogaster [34,35]. Our transcriptional result rather leads to the hypothesis that this pk2b2 allele is involved in the feminization of isopod hosts.…”

Section: Discussionmentioning

confidence: 41%

The expression of one ankyrin pk2 allele of the WO prophage is correlated with the Wolbachia feminizing effect in isopods

et al. 2012

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BackgroundThe maternally inherited α-Proteobacteria Wolbachia pipientis is an obligate endosymbiont of nematodes and arthropods, in which they induce a variety of reproductive alterations, including Cytoplasmic Incompatibility (CI) and feminization. The genome of the feminizing wVulC Wolbachia strain harboured by the isopod Armadillidium vulgare has been sequenced and is now at the final assembly step. It contains an unusually high number of ankyrin motif-containing genes, two of which are homologous to the phage-related pk1 and pk2 genes thought to contribute to the CI phenotype in Culex pipiens. These genes encode putative bacterial effectors mediating Wolbachia-host protein-protein interactions via their ankyrin motifs.ResultsTo test whether these Wolbachia homologs are potentially involved in altering terrestrial isopod reproduction, we determined the distribution and expression of both pk1 and pk2 genes in the 3 Wolbachia strains that induce CI and in 5 inducing feminization of their isopod hosts. Aside from the genes being highly conserved, we found a substantial copy number variation among strains, and that is linked to prophage diversity. Transcriptional analyses revealed expression of one pk2 allele (pk2b2) only in the feminizing Wolbachia strains of isopods.ConclusionsThese results reveal the need to investigate the functions of Wolbachia ankyrin gene products, in particular those of Pk2, and their host targets with respect to host sex manipulation.

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Section: Discussionmentioning

confidence: 41%

The expression of one ankyrin pk2 allele of the WO prophage is correlated with the Wolbachia feminizing effect in isopods

et al. 2012

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“…Although tissue-specific regulation of ankyrin domain-encoding genes by the parasitic endosymbiont Wolbachia within the gonads of multiple Drosophila spp. has been observed, these were also at comparably low levels (49). We examined the expression of two genes, thiC and hemH , associated with thiamine and heme biosynthesis; respectively, which are thought to be involved in host nutrient supplementation.…”

Section: Discussionmentioning

confidence: 86%

Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont Wigglesworthia

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Symula

Wang

et al. 2012

mBio

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Ancient endosymbionts have been associated with extreme genome structural stability with little differentiation in gene inventory between sister species. Tsetse flies (Diptera: Glossinidae) harbor an obligate endosymbiont, Wigglesworthia, which has coevolved with the Glossina radiation. We report on the ~720-kb Wigglesworthia genome and its associated plasmid from Glossina morsitans morsitans and compare them to those of the symbiont from Glossina brevipalpis. While there was overall high synteny between the two genomes, a large inversion was noted. Furthermore, symbiont transcriptional analyses demonstrated host tissue and development-specific gene expression supporting robust transcriptional regulation in Wigglesworthia, an unprecedented observation in other obligate mutualist endosymbionts. Expression and immunohistochemistry confirmed the role of flagella during the vertical transmission process from mother to intrauterine progeny. The expression of nutrient provisioning genes (thiC and hemH) suggests that Wigglesworthia may function in dietary supplementation tailored toward host development. Furthermore, despite extensive conservation, unique genes were identified within both symbiont genomes that may result in distinct metabolomes impacting host physiology. One of these differences involves the chorismate, phenylalanine, and folate biosynthetic pathways, which are uniquely present in Wigglesworthia morsitans. Interestingly, African trypanosomes are auxotrophs for phenylalanine and folate and salvage both exogenously. It is possible that W. morsitans contributes to the higher parasite susceptibility of its host species.

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“…This overrepresentation of ANK proteins in CI-inducing but only distantly related Cardinium and Wolbachia strains suggests that this class of proteins comprises important mediators of host cell interaction possibly involved in CI. Indeed, it has been frequently suggested earlier that ANK proteins could play a role in Wolbachia CI [22], [67], although the evidence has been equivocal [19], [68].…”

Section: Resultsmentioning

confidence: 99%

Comparative Genomics Suggests an Independent Origin of Cytoplasmic Incompatibility in Cardinium hertigii

et al. 2012

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Terrestrial arthropods are commonly infected with maternally inherited bacterial symbionts that cause cytoplasmic incompatibility (CI). In CI, the outcome of crosses between symbiont-infected males and uninfected females is reproductive failure, increasing the relative fitness of infected females and leading to spread of the symbiont in the host population. CI symbionts have profound impacts on host genetic structure and ecology and may lead to speciation and the rapid evolution of sex determination systems. Cardinium hertigii, a member of the Bacteroidetes and symbiont of the parasitic wasp Encarsia pergandiella, is the only known bacterium other than the Alphaproteobacteria Wolbachia to cause CI. Here we report the genome sequence of Cardinium hertigii cEper1. Comparison with the genomes of CI–inducing Wolbachia pipientis strains wMel, wRi, and wPip provides a unique opportunity to pinpoint shared proteins mediating host cell interaction, including some candidate proteins for CI that have not previously been investigated. The genome of Cardinium lacks all major biosynthetic pathways but harbors a complete biotin biosynthesis pathway, suggesting a potential role for Cardinium in host nutrition. Cardinium lacks known protein secretion systems but encodes a putative phage-derived secretion system distantly related to the antifeeding prophage of the entomopathogen Serratia entomophila. Lastly, while Cardinium and Wolbachia genomes show only a functional overlap of proteins, they show no evidence of laterally transferred elements that would suggest common ancestry of CI in both lineages. Instead, comparative genomics suggests an independent evolution of CI in Cardinium and Wolbachia and provides a novel context for understanding the mechanistic basis of CI.

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Regulation of Wolbachia ankyrin domain encoding genes in Drosophila gonads

Cited by 28 publications

References 55 publications

The expression of one ankyrin pk2 allele of the WO prophage is correlated with the Wolbachia feminizing effect in isopods

The expression of one ankyrin pk2 allele of the WO prophage is correlated with the Wolbachia feminizing effect in isopods

Insight into the Transmission Biology and Species-Specific Functional Capabilities of Tsetse (Diptera: Glossinidae) Obligate Symbiont Wigglesworthia

Comparative Genomics Suggests an Independent Origin of Cytoplasmic Incompatibility in Cardinium hertigii

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