IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52566-1.html
   My bibliography  Save this article

Gut symbiont-derived sphingosine modulates vector competence in Aedes mosquitoes

Author

Listed:
  • Xiaomei Sun

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

  • Yanhong Wang

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

  • Fei Yuan

    (Chinese Academy of Sciences)

  • Yanan Zhang

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

  • Xun Kang

    (Hainan Medical University)

  • Jian Sun

    (Chinese Academy of Sciences)

  • Pengcheng Wang

    (Chinese Academy of Sciences)

  • Tengfei Lu

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

  • Fanny Sae Wang

    (Mahidol University)

  • Jinbao Gu

    (Southern Medical University)

  • Jinglin Wang

    (Yunnan Animal Science and Veterinary Institute)

  • Qianfeng Xia

    (Hainan Medical University)

  • Aihua Zheng

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

  • Zhen Zou

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

Abstract

The main vectors of Zika virus (ZIKV) and dengue virus (DENV) are Aedes aegypti and Ae. albopictus, with Ae. aegypti being more competent. However, the underlying mechanisms remain unclear. Here, we find Ae. albopictus shows comparable vector competence to ZIKV/DENV with Ae. aegypti by blood-feeding after antibiotic treatment or intrathoracic injection. This suggests that midgut microbiota can influence vector competence. Enterobacter hormaechei_B17 (Eh_B17) is isolated from field-collected Ae. albopictus and conferred resistance to ZIKV/DENV infection in Ae. aegypti after gut-transplantation. Sphingosine, a metabolite secreted by Eh_B17, effectively suppresses ZIKV infection in both Ae. aegypti and cell cultures by blocking viral entry during the fusion step, with an IC50 of approximately 10 μM. A field survey reveals that Eh_B17 preferentially colonizes Ae. albopictus compared to Ae. aegypti. And field Ae. albopictus positive for Eh_B17 are more resistant to ZIKV infection. These findings underscore the potential of gut symbiotic bacteria, such as Eh_B17, to modulate the arbovirus vector competence of Aedes mosquitoes. As a natural antiviral agent, Eh_B17 holds promise as a potential candidate for blocking ZIKV/DENV transmission.

Suggested Citation

  • Xiaomei Sun & Yanhong Wang & Fei Yuan & Yanan Zhang & Xun Kang & Jian Sun & Pengcheng Wang & Tengfei Lu & Fanny Sae Wang & Jinbao Gu & Jinglin Wang & Qianfeng Xia & Aihua Zheng & Zhen Zou, 2024. "Gut symbiont-derived sphingosine modulates vector competence in Aedes mosquitoes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52566-1
    DOI: 10.1038/s41467-024-52566-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52566-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-52566-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Xiaoying Zheng & Dongjing Zhang & Yongjun Li & Cui Yang & Yu Wu & Xiao Liang & Yongkang Liang & Xiaoling Pan & Linchao Hu & Qiang Sun & Xiaohua Wang & Yingyang Wei & Jian Zhu & Wei Qian & Ziqiang Yan , 2019. "Incompatible and sterile insect techniques combined eliminate mosquitoes," Nature, Nature, vol. 572(7767), pages 56-61, August.
    2. Judith Lang & Patrick Bohn & Hilal Bhat & Holger Jastrow & Bernd Walkenfort & Feyza Cansiz & Julian Fink & Michael Bauer & Dominik Olszewski & Ana Ramos-Nascimento & Vikas Duhan & Sarah-Kim Friedrich , 2020. "Acid ceramidase of macrophages traps herpes simplex virus in multivesicular bodies and protects from severe disease," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    3. Elizabeth L. Johnson & Stacey L. Heaver & Jillian L. Waters & Benjamin I. Kim & Alexis Bretin & Andrew L. Goodman & Andrew T. Gewirtz & Tilla S. Worgall & Ruth E. Ley, 2020. "Sphingolipids produced by gut bacteria enter host metabolic pathways impacting ceramide levels," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. Thomas Obadia & Gladys Gutierrez-Bugallo & Veasna Duong & Ana I. Nuñez & Rosilainy S. Fernandes & Basile Kamgang & Liza Hery & Yann Gomard & Sandra R. Abbo & Davy Jiolle & Uros Glavinic & Myrielle Dup, 2022. "Zika vector competence data reveals risks of outbreaks: the contribution of the European ZIKAlliance project," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    5. Xiaomei Sun & Xueli Wang & Kai Shi & Xiangyang Lyu & Jian Sun & Alexander S. Raikhel & Zhen Zou, 2024. "Leucine aminopeptidase1 controls egg deposition and hatchability in male Aedes aegypti mosquitoes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. W. Robert Shaw & Perrine Marcenac & Lauren M. Childs & Caroline O. Buckee & Francesco Baldini & Simon P. Sawadogo & Roch K. Dabiré & Abdoulaye Diabaté & Flaminia Catteruccia, 2016. "Wolbachia infections in natural Anopheles populations affect egg laying and negatively correlate with Plasmodium development," Nature Communications, Nature, vol. 7(1), pages 1-7, September.
    7. A. A. Hoffmann & B. L. Montgomery & J. Popovici & I. Iturbe-Ormaetxe & P. H. Johnson & F. Muzzi & M. Greenfield & M. Durkan & Y. S. Leong & Y. Dong & H. Cook & J. Axford & A. G. Callahan & N. Kenny & , 2011. "Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission," Nature, Nature, vol. 476(7361), pages 454-457, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xingtong Liu & Yuanshun Tan & Bo Zheng, 2022. "Dynamic Behavior of an Interactive Mosquito Model under Stochastic Interference," Mathematics, MDPI, vol. 10(13), pages 1-18, June.
    2. Zhongcai Zhu & Yantao Shi & Rong Yan & Linchao Hu, 2022. "Periodic Orbits of a Mosquito Suppression Model Based on Sterile Mosquitoes," Mathematics, MDPI, vol. 10(3), pages 1-21, January.
    3. Yijie Li & Zhiming Guo, 2022. "Wolbachia Invasion Dynamics by Integrodifference Equations," Mathematics, MDPI, vol. 10(22), pages 1-13, November.
    4. Lijie Chang & Yantao Shi & Bo Zheng, 2021. "Existence and Uniqueness of Nontrivial Periodic Solutions to a Discrete Switching Model," Mathematics, MDPI, vol. 9(19), pages 1-13, September.
    5. Auliya A. Suwantika & Angga P. Kautsar & Woro Supadmi & Neily Zakiyah & Rizky Abdulah & Mohammad Ali & Maarten J. Postma, 2020. "Cost-Effectiveness of Dengue Vaccination in Indonesia: Considering Integrated Programs with Wolbachia -Infected Mosquitos and Health Education," IJERPH, MDPI, vol. 17(12), pages 1-15, June.
    6. Marcel Rühling & Louise Kersting & Fabienne Wagner & Fabian Schumacher & Dominik Wigger & Dominic A. Helmerich & Tom Pfeuffer & Robin Elflein & Christian Kappe & Markus Sauer & Christoph Arenz & Burkh, 2024. "Trifunctional sphingomyelin derivatives enable nanoscale resolution of sphingomyelin turnover in physiological and infection processes via expansion microscopy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Rabindra K. Mandal & Anita Mandal & Joshua E. Denny & Ruth Namazii & Chandy C. John & Nathan W. Schmidt, 2023. "Gut Bacteroides act in a microbial consortium to cause susceptibility to severe malaria," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Martin Foureaux Koppensteiner & Lívia Menezes, 2024. "Maternal Dengue and Health Outcomes of Children," American Economic Journal: Applied Economics, American Economic Association, vol. 16(2), pages 530-553, April.
    9. Qiming Huang & Lijie Chang & Zhaowang Zhang & Bo Zheng, 2023. "Global Dynamics for Competition between Two Wolbachia Strains with Bidirectional Cytoplasmic Incompatibility," Mathematics, MDPI, vol. 11(7), pages 1-21, April.
    10. Philipp Walch & Petr Broz, 2024. "Viral-bacterial co-infections screen in vitro reveals molecular processes affecting pathogen proliferation and host cell viability," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Gaelle Gabiane & Chloé Bohers & Laurence Mousson & Thomas Obadia & Rhoel R. Dinglasan & Marie Vazeille & Catherine Dauga & Marine Viglietta & André Yébakima & Anubis Vega-Rúa & Gladys Gutiérrez Bugall, 2024. "Evaluating vector competence for Yellow fever in the Caribbean," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    12. Dongjing Zhang & Hamidou Maiga & Yongjun Li & Mame Thierno Bakhoum & Gang Wang & Yan Sun & David Damiens & Wadaka Mamai & Nanwintoum Séverin Bimbilé Somda & Thomas Wallner & Odet Bueno-Masso & Claudia, 2024. "Mating harassment may boost the effectiveness of the sterile insect technique for Aedes mosquitoes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    13. Turelli, Michael & Barton, Nicholas H., 2017. "Deploying dengue-suppressing Wolbachia : Robust models predict slow but effective spatial spread in Aedes aegypti," Theoretical Population Biology, Elsevier, vol. 115(C), pages 45-60.
    14. Kristina K. Gonzales & Immo A. Hansen, 2016. "Artificial Diets for Mosquitoes," IJERPH, MDPI, vol. 13(12), pages 1-13, December.
    15. Isaac G. Crusoe & Ian C. Chiwaya & Tasnim I. Habib, 2024. "Immune Control of Gut Microbiota Prevents Obesity and the Effect of Antibiotic on Microbial Population," International Journal of Research and Scientific Innovation, International Journal of Research and Scientific Innovation (IJRSI), vol. 11(5), pages 1-9, May.
    16. Chloé Hérault & Thomas Pihl & Bruno Hudry, 2024. "Cellular sex throughout the organism underlies somatic sexual differentiation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    17. Li Ting Soh & Zoe Ong & Kathryn Vasquez & Irene Chen & Xiaoxi Li & Weixin Niah & Chitra Panchapakesan & Anita Sheldenkar & Shuzhen Sim & Lee Ching Ng & May O. Lwin, 2021. "A Household-Based Survey to Understand Factors Influencing Awareness, Attitudes and Knowledge towards Wolbachia-Aedes Technology," IJERPH, MDPI, vol. 18(22), pages 1-16, November.
    18. Rachel Lowe & Christovam Barcellos & Patrícia Brasil & Oswaldo G. Cruz & Nildimar Alves Honório & Hannah Kuper & Marilia Sá Carvalho, 2018. "The Zika Virus Epidemic in Brazil: From Discovery to Future Implications," IJERPH, MDPI, vol. 15(1), pages 1-18, January.
    19. Ayu Rahayu & Utari Saraswati & Endah Supriyati & Dian Aruni Kumalawati & Rio Hermantara & Anwar Rovik & Edwin Widyanto Daniwijaya & Iva Fitriana & Sigit Setyawan & Riris Andono Ahmad & Dwi Satria Ward, 2019. "Prevalence and Distribution of Dengue Virus in Aedes aegypti in Yogyakarta City before Deployment of Wolbachia Infected Aedes aegypti," IJERPH, MDPI, vol. 16(10), pages 1-12, May.
    20. Tiago França Melo De Lima & Raquel Martins Lana & Tiago Garcia De Senna Carneiro & Cláudia Torres Codeço & Gabriel Souza Machado & Lucas Saraiva Ferreira & Líliam César De Castro Medeiros & Clodoveu A, 2016. "DengueME: A Tool for the Modeling and Simulation of Dengue Spatiotemporal Dynamics," IJERPH, MDPI, vol. 13(9), pages 1-21, September.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52566-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.