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Transgenic expression of cif genes from Wolbachia strain wAlbB recapitulates cytoplasmic incompatibility in Aedes aegypti

Author

Listed:
  • Cameron J. McNamara

    (MRC—University of Glasgow Centre for Virus Research)

  • Thomas H. Ant

    (MRC—University of Glasgow Centre for Virus Research)

  • Tim Harvey-Samuel

    (The Pirbright Institute)

  • Helen White-Cooper

    (Cardiff University)

  • Julien Martinez

    (MRC—University of Glasgow Centre for Virus Research)

  • Luke Alphey

    (The Pirbright Institute
    University of York)

  • Steven P. Sinkins

    (MRC—University of Glasgow Centre for Virus Research)

Abstract

The endosymbiotic bacteria Wolbachia can invade insect populations by modifying host reproduction through cytoplasmic incompatibility (CI), an effect that results in embryonic lethality when Wolbachia-carrying males mate with Wolbachia-free females. Here we describe a transgenic system for recreating CI in the major arbovirus vector Aedes aegypti using CI factor (cif) genes from wAlbB, a Wolbachia strain currently being deployed to reduce dengue transmission. CI-like sterility is induced when cifA and cifB are co-expressed in testes; this sterility is rescued by maternal cifA expression, thereby reproducing the pattern of Wolbachia-induced CI. Expression of cifB alone is associated with extensive DNA damage and disrupted spermatogenesis. The strength of rescue by maternal cifA expression is dependent on the comparative levels of cifA/cifB expression in males. These findings are consistent with CifB acting as a toxin and CifA as an antitoxin, with CifA attenuating CifB toxicity in both the male germline and in developing embryos. These findings provide important insights into the interactions between cif genes and their mechanism of activity and provide a foundation for the building of a cif gene-based drive system in Ae. aegypti.

Suggested Citation

  • Cameron J. McNamara & Thomas H. Ant & Tim Harvey-Samuel & Helen White-Cooper & Julien Martinez & Luke Alphey & Steven P. Sinkins, 2024. "Transgenic expression of cif genes from Wolbachia strain wAlbB recapitulates cytoplasmic incompatibility in Aedes aegypti," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45238-7
    DOI: 10.1038/s41467-024-45238-7
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    References listed on IDEAS

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    1. Haofeng Wang & Yunjie Xiao & Xia Chen & Mengwen Zhang & Guangxin Sun & Feng Wang & Lin Wang & Hanxiao Zhang & Xiaoyu Zhang & Xin Yang & Wenling Li & Yi Wei & Deqiang Yao & Bing Zhang & Jun Li & Wen Cu, 2022. "Crystal Structures of Wolbachia CidA and CidB Reveal Determinants of Bacteria-induced Cytoplasmic Incompatibility and Rescue," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Daniel P. LePage & Jason A. Metcalf & Sarah R. Bordenstein & Jungmin On & Jessamyn I. Perlmutter & J. Dylan Shropshire & Emily M. Layton & Lisa J. Funkhouser-Jones & John F. Beckmann & Seth R. Bordens, 2017. "Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility," Nature, Nature, vol. 543(7644), pages 243-247, March.
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