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Outer membrane vesicles from a mosquito commensal mediate targeted killing of Plasmodium parasites via the phosphatidylcholine scavenging pathway

Author

Listed:
  • Han Gao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yongmao Jiang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Lihua Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Guandong Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Wenqian Hu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Ling Dong

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Sibao Wang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

The gut microbiota is a crucial modulator of Plasmodium infection in mosquitoes, including the production of anti-Plasmodium effector proteins. But how the commensal-derived effectors are translocated into Plasmodium parasites remains obscure. Here we show that a natural Plasmodium blocking symbiotic bacterium Serratia ureilytica Su_YN1 delivers the effector lipase AmLip to Plasmodium parasites via outer membrane vesicles (OMVs). After a blood meal, host serum strongly induces Su_YN1 to release OMVs and the antimalarial effector protein AmLip into the mosquito gut. AmLip is first secreted into the extracellular space via the T1SS and then preferentially loaded on the OMVs that selectively target the malaria parasite, leading to targeted killing of the parasites. Notably, these serum-induced OMVs incorporate certain serum-derived lipids, such as phosphatidylcholine, which is critical for OMV uptake by Plasmodium via the phosphatidylcholine scavenging pathway. These findings reveal that this gut symbiotic bacterium evolved to deliver secreted effector molecules in the form of extracellular vesicles to selectively attack parasites and render mosquitoes refractory to Plasmodium infection. The discovery of the role of gut commensal-derived OMVs as carriers in cross-kingdom communication between mosquito microbiota and Plasmodium parasites offers a potential innovative strategy for blocking malaria transmission.

Suggested Citation

  • Han Gao & Yongmao Jiang & Lihua Wang & Guandong Wang & Wenqian Hu & Ling Dong & Sibao Wang, 2023. "Outer membrane vesicles from a mosquito commensal mediate targeted killing of Plasmodium parasites via the phosphatidylcholine scavenging pathway," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40887-6
    DOI: 10.1038/s41467-023-40887-6
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    References listed on IDEAS

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    1. Jackie L. Shane & Christina L. Grogan & Caroline Cwalina & David J. Lampe, 2018. "Blood meal-induced inhibition of vector-borne disease by transgenic microbiota," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    2. Enrique R. Rojas & Gabriel Billings & Pascal D. Odermatt & George K. Auer & Lillian Zhu & Amanda Miguel & Fred Chang & Douglas B. Weibel & Julie A. Theriot & Kerwyn Casey Huang, 2018. "The outer membrane is an essential load-bearing element in Gram-negative bacteria," Nature, Nature, vol. 559(7715), pages 617-621, July.
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