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Wolbachia is a nutritional symbiont

View ORCID ProfileAmelia RI Lindsey, View ORCID ProfileAudrey J Parish, View ORCID ProfileIrene LG Newton, View ORCID ProfileJason M Tennessen, Megan W Jones, Nicole Stark
doi: https://doi.org/10.1101/2023.01.20.524972
Amelia RI Lindsey
1Department of Entomology, University of Minnesota, St. Paul, Minnesota, 55108
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  • For correspondence: alindsey@umn.edu
Audrey J Parish
2Department of Biology, Indiana University, Bloomington, Indiana, 47405
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Irene LG Newton
2Department of Biology, Indiana University, Bloomington, Indiana, 47405
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Jason M Tennessen
2Department of Biology, Indiana University, Bloomington, Indiana, 47405
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Megan W Jones
1Department of Entomology, University of Minnesota, St. Paul, Minnesota, 55108
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Nicole Stark
2Department of Biology, Indiana University, Bloomington, Indiana, 47405
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ABSTRACT

Approximately a quarter of eukaryotes are infected with the bacterium Wolbachia. Its broad success as a vertically transmitted infection has been historically difficult to explain given the myriad of parasitic impacts characterized across Wolbachia’s host range. Using the Drosophila model and their natively associated Wolbachia, we show that Wolbachia infection supports fly development and buffers against nutritional stress. Wolbachia infection across several fly genotypes and a range of nutrient conditions resulted in reduced pupal mortality, increased adult emergence, and larger size. We determined that the exogenous supplementation of pyrimidines rescued these phenotypes in the Wolbachia-free, flies suggesting that Wolbachia plays a role in providing this metabolite that is normally limiting for insect growth. Additionally, Wolbachia was sensitive to host pyrimidine metabolism: Wolbachia titers increased upon transgenic knockdown of the Drosophila de novo pyrimidine synthesis pathway but not knockdown of the de novo purine synthesis pathway. We propose that Wolbachia acts as a nutritional symbiont to supplement insect development and increase host fitness: a selective advantage that could contribute to its high frequency in nature.

SIGNIFICANCE STATEMENT Wolbachia is a bacterial symbiont of ∼1/4 of all eukaryotic species on earth, often deemed a “parasite” due to selfish manipulations of arthropod reproduction. However, many have theorized there must be more to this symbiosis: parasitic and reproductive impacts alone cannot explain the success and ubiquity of this bacterium. Here, we use Drosophila and their native Wolbachia infections to show that Wolbachia supports fly development and significantly buffers flies against nutritional stress. Additionally, we show that this advantage is likely mediated by pyrimidines: a biosynthetic pathway that all Wolbachia lineages encode for. These developmental advantages might help explain the ubiquity of Wolbachia infections.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted January 21, 2023.
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Wolbachia is a nutritional symbiont
Amelia RI Lindsey, Audrey J Parish, Irene LG Newton, Jason M Tennessen, Megan W Jones, Nicole Stark
bioRxiv 2023.01.20.524972; doi: https://doi.org/10.1101/2023.01.20.524972
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Wolbachia is a nutritional symbiont
Amelia RI Lindsey, Audrey J Parish, Irene LG Newton, Jason M Tennessen, Megan W Jones, Nicole Stark
bioRxiv 2023.01.20.524972; doi: https://doi.org/10.1101/2023.01.20.524972

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