Polyphenol-Rich Diets Exacerbate AMPK-Mediated Autophagy, Decreasing Proliferation of Mosquito Midgut Microbiota, and Extending Vector Lifespan

PLoS Negl Trop Dis. 2016 Oct 12;10(10):e0005034. doi: 10.1371/journal.pntd.0005034. eCollection 2016 Oct.

Abstract

Background: Mosquitoes feed on plant-derived fluids such as nectar and sap and are exposed to bioactive molecules found in this dietary source. However, the role of such molecules on mosquito vectorial capacity is unknown. Weather has been recognized as a major determinant of the spread of dengue, and plants under abiotic stress increase their production of polyphenols.

Results: Here, we show that including polyphenols in mosquito meals promoted the activation of AMP-dependent protein kinase (AMPK). AMPK positively regulated midgut autophagy leading to a decrease in bacterial proliferation and an increase in vector lifespan. Suppression of AMPK activity resulted in a 6-fold increase in midgut microbiota. Similarly, inhibition of polyphenol-induced autophagy induced an 8-fold increase in bacterial proliferation. Mosquitoes maintained on the polyphenol diet were readily infected by dengue virus.

Conclusion: The present findings uncover a new direct route by which exacerbation of autophagy through activation of the AMPK pathway leads to a more efficient control of mosquito midgut microbiota and increases the average mosquito lifespan. Our results suggest for the first time that the polyphenol content and availability of the surrounding vegetation may increase the population of mosquitoes prone to infection with arboviruses.

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism*
  • Aedes / enzymology
  • Aedes / growth & development
  • Aedes / metabolism
  • Aedes / microbiology*
  • Animal Feed / analysis
  • Animals
  • Autophagy*
  • Bacteria / classification
  • Bacteria / genetics
  • Bacteria / growth & development*
  • Bacteria / isolation & purification
  • Female
  • Gastrointestinal Microbiome
  • Gastrointestinal Tract* / microbiology
  • Gastrointestinal Tract* / physiology
  • Insect Proteins / genetics
  • Insect Proteins / metabolism*
  • Insect Vectors / enzymology
  • Insect Vectors / growth & development
  • Insect Vectors / metabolism
  • Insect Vectors / microbiology*
  • Male
  • Polyphenols / metabolism*

Substances

  • Insect Proteins
  • Polyphenols
  • AMP-Activated Protein Kinases

Grants and funding

This work was supported by Fundação Carlos Chagas Filho de Apoio a Pesquisa do Estado do Rio de Janeiro (FAPERJ) through the following grant E-26/103.092/2011. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.