Abstract

Mosquitoes acquire the pathogens they transmit through ingestion, and the insects’ gut constitutes the first line of defense against invading pathogens. Indeed the gut epithelium acts as a physical barrier, activates local antimicrobial peptides production and triggers the systemic immune response. Consequently, gut epithelium is constantly confronted to stress and often suffers cellular damage. We have previously shown that regenerative cells are present in the guts of adult Aedes albopictus, and that chemical damage or bacterial infection leads to the proliferation of these regenerative cells in the midgut. In this study, we extended the analysis of gut cells response to stress to two other important disease vector mosquitoes: Culex pipiens and Anopheles gambiae. We fed mosquitoes on sucrose solutions or on sucrose supplemented with pathogenic bacteria or with damage-inducing chemicals. We also assayed the survival of mosquitoes following the ingestion of pathogenic bacteria. We found that in adult C. pipiens, dividing cells exist in the digestive tract and that these cells proliferate in the midgut after bacterial or chemical damage, similarly to what we previously observed in A. albopictus. In sharp contrast, we did not detect any mitotic cell in the midguts of A. gambiae mosquitoes, neither in normal situation nor after the induction of gut damage. In agreement with this observation, A. gambiae mosquitoes were more sensitive to oral bacterial infections compared to A. albopictus and C. pipiens. This work provides evidence that major differences in gut physiological responses exist between different mosquitoes. The presence of regenerative cells in the mosquito guts and their ability to multiply after gut damage affect the mosquito survival to oral infections, and is also likely to affect its vectorial capacity.

Highlights

  • Results in a massive loss of enterocytes[17]

  • We found that in adult C. pipiens, dividing cells exist in the digestive tract and that these cells proliferate in the midgut after the ingestion of pathogenic bacterial or damaging chemicals, to what we previously observed in A. albopictus

  • We found an important dissimilarity between the different mosquitoes’ response to gut damage: we did not detect any mitotic cell in the midguts of A. gambiae mosquitoes, neither in normal situation nor after the induction of gut damage, while in C. pipiens, dividing cells exist in the digestive tract and proliferate in the midgut after bacterial or chemical damage, to what was previously observed in A. albopictus[25] and A. aegypti[26]

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Summary

Introduction

Homeostatic repair pathways leading to the preservation of epithelial integrity are activated This involves the regulation of intestinal stem cells (ISCs) that are necessary for gut regeneration. In Drosophila melanogaster, ISCs can proliferate quickly and massively so that enterocytes are completely regenerated in less than 60 hours in damaged midguts[17,18,19]. We have shown that chemical damage or bacterial infections lead to regenerative cell proliferation in the midgut of adult A. albopictus[25]. We extended the analysis of adult gut regeneration to two other important disease vector mosquitoes: C. pipiens and A. gambiae. We found that in adult C. pipiens, dividing cells exist in the digestive tract and that these cells proliferate in the midgut after the ingestion of pathogenic bacterial or damaging chemicals, to what we previously observed in A. albopictus. We expect the results of this study to have implications for vector control methods

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