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Comparative genomics of closely related Wolbachia strains infecting Drosophila
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution.
IAEA Division of Nuclear Techniques in Food and Agriculture.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Cytoplasmic incompatibility (CI) is the most common form of reproductive manipulation induced by the vertically inherited endosymbiont Wolbachia. The phenotype causes partial or complete sterility in crosses between infected males and non-infected females, thus benefiting infected females in the population and the spread of the bacteria. Because of these properties, CI-inducing Wolbachia has been implicated as a mean for biological pest control. Although CI has been known for several decades, the first CI-associated genes, cifA and cifB, were only recently discovered. In this study, we sequenced five complete Wolbachia genomes (wSan, wYak, wTei, wAu, wMa,) and performed comparative genomic analyses between these and four previously published complete Wolbachia genomes (wRi, wNo, wHa, wMel), that have all had their CI properties tested in the same genetic host background, Drosophila simulans STC. Using these genomes, we investigate what types of genes differ between closely related Wolbachia strains and compare the sequences from some of the strains in their natural host vs. after transfer to D. simulans STC. We find that phage-associated and hypothetical genes are likely to vary more between genomes and that very few mutations have occurred when strains were transferred to D. simulans. Furthermore, we investigate the evolution of the known CI genes and take advantage of the highly similar genomes of some strains as well as their complex CI properties to identify further genes associated with both mod and resc functions of CI.

National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
URN: urn:nbn:se:uu:diva-406756OAI: oai:DiVA.org:uu-406756DiVA, id: diva2:1414021
Available from: 2020-03-11 Created: 2020-03-11 Last updated: 2020-03-12
In thesis
1. Genomic and transcriptomic investigation of reproductive incompatibility in Drosophila
Open this publication in new window or tab >>Genomic and transcriptomic investigation of reproductive incompatibility in Drosophila
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Both nuclear and cytoplasmic elements can contribute to the emergence of reproductive incompatibilities that influence evolution and speciation. In the projects that compose this thesis, we use genomics and transcriptomics to study some of those elements in Drosophila.

In the first study, we show that Wolbachia, an endosymbiotic bacterium known to cause reproductive alterations in its hosts, influences gene expression in D. paulistorum. Affected genes were associated with biological functions such as metabolism, immunity, reproduction, and chemical communication. Our results indicate that Wolbachia accentuates the differences in expression profiles between semispecies and suggest that the symbiont influences host pre-and postmating isolation.

In the second paper, we uncover widespread persistent heteroplasmy in D. paulistorum. We reveal that D. paulistorum mitochondria are polyphyletic, with two divergent mitotypes, and that the heteroplasmy likely originated through introgression. One of the mitotypes shows biparental inheritance, non-responsiveness to host energy demands and rapid titer increase in the early embryo. We hypothesize that such selfish traits evolved in response to competition between mitotypes.

In the third project, we show that differentially expressed genes between D. paulistorum semispecies are associated with a variety of biological processes, especially broad regulatory functions that occur via variability in transcription, translation and ubiquitination of post-translational modification. We reveal that the expression profile of F1 inter-semispecies hybrids is markedly similar to that of the maternal line, and that Wolbachia has a small but potentially significant interaction with genes that are differentially expressed in semispecies and F1 hybrids.

Finally, we use comparative genomics to study the evolution of closely related Wolbachia strains with known reproductive phenotypes. We confirm previous observations that Wolbachia genomes are very dynamic and that phage-associated regions are particularly variable and likely involved in horizontal transfer of genes linked to reproductive phenotypes. An in-depth screen for genetic elements potentially involved in Wolbachia-induced cytoplasmic incompatibility recovers genes previously known to be involved in the phenotype and novel candidates.

In conclusion, this thesis contributes to our understanding of genetic factors that affect Drosophila evolution, particularly those leading to reproductive incompatibility in D. paulistorum and associated with Wolbachia.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2020. p. 69
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1914
Keywords
Wolbachia, Drosophila, Drosophila paulistorum, Differential Gene Expression, Reproductive Incompatibility, Reproductive Isolation, Comparative Genomics, Transcriptomics, RNA-Seq, Heteroplasmy, Mitochondria, Genomic conflict
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
urn:nbn:se:uu:diva-406758 (URN)978-91-513-0897-5 (ISBN)
Public defence
2020-04-24, Room A1:111a, BMC, Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2020-04-02 Created: 2020-03-12 Last updated: 2020-05-19

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Baiao, Guilherme CostaKlasson, Lisa

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