A transcriptomic atlas of Aedes aegypti reveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females

Abstract

Mosquito vectors transmit numerous pathogens, but large gaps remain in our understanding of their physiology. To facilitate future explorations of mosquito biology, with specific attention to the major vector Aedes aegypti, we have created Aegypti-Atlas (http://aegyptiatlas.buchonlab.com/), an online resource hosting RNAseq profiles of Ae. aegypti body parts (head, thorax, abdomen, gut, Malpighian tubules, and ovaries), gut regions (crop, proventriculus, anterior and posterior midgut, and hindgut), and a time course of blood meal digestion in the gut. Using Aegypti-Atlas, we provide new insights into the regionalization of gut function, blood feeding response, and immune defenses. We find that the anterior and posterior regions of the mosquito midgut possess clearly delineated digestive specializations which are preserved in the blood-fed state. Blood feeding initiates the sequential transcriptional induction and repression/depletion of multiple cohorts of peptidases throughout blood meal digestion. With respect to defense, immune signaling components, but not recognition or effector molecules, show enrichment in ovaries. Basal expression of antimicrobial peptides is dominated by two genes, holotricin and gambicin, that are expressed in the carcass and the digestive tissues, respectively, in a near mutually exclusive manner. In the midgut, gambicin and other immune effector genes are almost exclusively expressed in the anterior regions, while the posterior midgut exhibits the hallmarks of immune tolerance. Finally, in a cross-species comparison between the midguts of Ae. aegypti and Anopheles gambiae (s.l.), we observe that regional digestive and immune specializations are closely conserved, indicating that our data may yield inferences that are broadly relevant to multiple mosquito vector species. We further demonstrate that the expression of orthologous genes is highly correlated, with the exception of a ‘species signature’ comprising a small number of highly/disparately expressed genes. With this work, we show the potential of Aegypti-Atlas to unlock a more complete understanding of mosquito biology.

Data availability

Data have been submitted to NCBI. The BioProject ID is PRJNA789580

The following data sets were generated

Article and author information

Author details

  1. Bretta Hixson

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Xiao-Li Bing

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Xiaowei Yang

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alessandro Bonfini

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6642-8665
  5. Peter Nagy

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5053-0646
  6. Nicolas Buchon

    Department of Entomology, Cornell University, Ithaca, United States
    For correspondence
    nicolas.buchon@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3636-8387

Funding

National Institute of Allergy and Infectious Diseases (1R01AI148529-02)

  • Nicolas Buchon

National Science Foundation (IOS 2024252)

  • Nicolas Buchon

National Institute of Allergy and Infectious Diseases (1R01AI148541-02)

  • Nicolas Buchon

National Institute on Aging (5R21AG065733-02)

  • Nicolas Buchon

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Bruno Lemaître, École Polytechnique Fédérale de Lausanne, Switzerland

Publication history

  1. Received: December 6, 2021
  2. Preprint posted: December 21, 2021 (view preprint)
  3. Accepted: April 25, 2022
  4. Accepted Manuscript published: April 26, 2022 (version 1)
  5. Version of Record published: May 17, 2022 (version 2)

Copyright

© 2022, Hixson et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Bretta Hixson
  2. Xiao-Li Bing
  3. Xiaowei Yang
  4. Alessandro Bonfini
  5. Peter Nagy
  6. Nicolas Buchon
(2022)
A transcriptomic atlas of Aedes aegypti reveals detailed functional organization of major body parts and gut regional specializations in sugar-fed and blood-fed adult females
eLife 11:e76132.
https://doi.org/10.7554/eLife.76132
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