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Holobiont perspectives on tripartite interactions among microbiota, mosquitoes, and pathogens

The ISME Journal (2023)Cite this article

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Abstract

Mosquito-borne diseases like dengue and malaria cause a significant global health burden. Unfortunately, current insecticides and environmental control strategies aimed at the vectors of these diseases are only moderately effective in decreasing disease burden. Understanding and manipulating the interaction between the mosquito holobiont (i.e., mosquitoes and their resident microbiota) and the pathogens transmitted by these mosquitoes to humans and animals could help in developing new disease control strategies. Different microorganisms found in the mosquito’s microbiota affect traits related to mosquito survival, development, and reproduction. Here, we review the physiological effects of essential microbes on their mosquito hosts; the interactions between the mosquito holobiont and mosquito-borne pathogen (MBP) infections, including microbiota-induced host immune activation and Wolbachia-mediated pathogen blocking (PB); and the effects of environmental factors and host regulation on the composition of the microbiota. Finally, we briefly overview future directions in holobiont studies, and how these may lead to new effective control strategies against mosquitoes and their transmitted diseases.

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Fig. 1: Mosquito holobiont: the chimera of the mosquito, its microbiota, and interactions between them.
Fig. 2: Schematic diagram of the microbiota-mosquito-pathogen interactions.
Fig. 3: Schematic representation of the acquisition and composition of mosquito microbiota.
Fig. 4: Strategies of holobiont manipulation for mosquito control and pathogen transmission.

Data availability

The data that support the findings of this study are available from the corresponding author, Guan-Hong Wang, upon reasonable request.

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Acknowledgements

This work was supported by the CAS strategic funding via CAS-CSIRO funding scheme (152111KYSB20210011), the National Key R&D Program of China (2022YFF0710603), the National Science Foundation of China (32270538), and the Natural Science Foundation of Beijing (6222046) awarded to G.H.W. The work was also supported by CSIRO strategic funding via CAS-CSIRO funding scheme to PNP. We thank Lei Jiang and Wenxin Ma for their helpful edits on earlier versions of Figs. 2 and 3.

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  1. These authors contributed equally: Ronger Zheng, Qiqi Wang, Runbiao Wu.

Authors and Affiliations

  1. State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

    Ronger Zheng, Qiqi Wang, Runbiao Wu & Guan-Hong Wang

  2. University of Chinese Academy of Sciences, Beijing, China

    Ronger Zheng

  3. CSIRO Health and Biosecurity, Australian Centre for Disease Preparedness, Geelong, VIC, Australia

    Prasad N. Paradkar

  4. Pest and Environmental Adaptation Research Group, Bio21 Institute and the School of BioSciences, The University of Melbourne, Parkville, VIC, Australia

    Ary A. Hoffmann

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  1. Ronger Zheng
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Zheng, R., Wang, Q., Wu, R. et al. Holobiont perspectives on tripartite interactions among microbiota, mosquitoes, and pathogens. ISME J (2023). https://doi.org/10.1038/s41396-023-01436-7

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