Bacteria-mediated hypoxia functions as a signal for mosquito development

Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):E5362-E5369. doi: 10.1073/pnas.1702983114. Epub 2017 Jun 19.

Abstract

Mosquitoes host communities of microbes in their digestive tract that consist primarily of bacteria. We previously reported that several mosquito species, including Aedes aegypti, do not develop beyond the first instar when fed a nutritionally complete diet in the absence of a gut microbiota. In contrast, several species of bacteria, including Escherichia coli, rescue development of axenic larvae into adults. The molecular mechanisms underlying bacteria-dependent growth are unknown. Here, we designed a genetic screen around E. coli that identified high-affinity cytochrome bd oxidase as an essential bacterial gene product for mosquito growth. Bioassays showed that bacteria in nonsterile larvae and gnotobiotic larvae inoculated with wild-type E. coli reduced midgut oxygen levels below 5%, whereas larvae inoculated with E. coli mutants defective for cytochrome bd oxidase did not. Experiments further supported that hypoxia leads to growth and ecdysone-induced molting. Altogether, our results identify aerobic respiration by bacteria as a previously unknown but essential process for mosquito development.

Keywords: bacteria; growth; hypoxia; insect; microbiota.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Culicidae / growth & development*
  • Culicidae / microbiology*
  • Cytochrome b Group
  • Cytochromes / genetics*
  • Cytochromes / metabolism
  • DNA, Bacterial / genetics
  • Electron Transport Chain Complex Proteins / genetics*
  • Electron Transport Chain Complex Proteins / metabolism
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Escherichia coli Proteins / genetics*
  • Escherichia coli Proteins / metabolism
  • Female
  • Fermentation*
  • Gastrointestinal Microbiome
  • Gastrointestinal Tract / microbiology
  • Germ-Free Life
  • Green Fluorescent Proteins / metabolism
  • Hydrogen-Ion Concentration
  • Hypoxia*
  • Larva / metabolism
  • Mutation
  • Open Reading Frames
  • Oxidoreductases / genetics*
  • Oxidoreductases / metabolism
  • Oxygen / metabolism
  • Prolyl Hydroxylases / metabolism

Substances

  • Cytochrome b Group
  • Cytochromes
  • DNA, Bacterial
  • Electron Transport Chain Complex Proteins
  • Escherichia coli Proteins
  • Green Fluorescent Proteins
  • Oxidoreductases
  • Prolyl Hydroxylases
  • cytochrome bd terminal oxidase complex, E coli
  • Oxygen