Internal amino acid state modulates yeast taste neurons to support protein homeostasis in Drosophila

Abstract

To optimize fitness, animals must dynamically match food choices to their current needs. For drosophilids, yeast fulfils most dietary protein and micronutrient requirements. While several yeast metabolites activate known gustatory receptor neurons (GRNs) in Drosophila melanogaster, the chemosensory channels mediating yeast feeding remain unknown. Here we identify a class of proboscis GRNs required for yeast intake. Within this class, taste peg GRNs are specifically required to sustain yeast feeding. Sensillar GRNs, however, mediate feeding initiation. Furthermore, the response of yeast GRNs, but not sweet GRNs, is enhanced following deprivation from amino acids, providing a potential basis for protein-specific appetite. Although nutritional and reproductive states synergistically increase yeast appetite, reproductive state acts independently of nutritional state, modulating processing downstream of GRNs. Together, these results suggest that different internal states act at distinct levels of a dedicated gustatory circuit to elicit nutrient-specific appetites towards a complex, ecologically relevant protein source.

Article and author information

Author details

  1. Kathrin Steck

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  2. Samuel J Walker

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  3. Pavel M Itskov

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    Pavel M Itskov, PMI has a commercial interest in the flyPAD open-source technology.
  4. Celia Baltazar

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  5. José-Maria Moreira

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    Competing interests
    No competing interests declared.
  6. Carlos Ribeiro

    Champalimaud Research, Champalimaud Centre for the Unknown, Lisbon, Portugal
    For correspondence
    carlos.ribeiro@neuro.fchampalimaud.org
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9542-7335

Funding

Fundação para a Ciência e a Tecnologia (PTDC/BIA-BCM/118684/2010)

  • Carlos Ribeiro

Fundação para a Ciência e a Tecnologia (SFRH/BPD/79325/2011)

  • Pavel M Itskov

Human Frontier Science Program (RGP0022/2012)

  • Carlos Ribeiro

Fundação Bial (283/14)

  • Carlos Ribeiro

Fundação Bial (279/16)

  • Carlos Ribeiro

European Commission (FLiACT ITN)

  • Carlos Ribeiro

Champalimaud Foundation

  • Carlos Ribeiro

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Version history

  1. Received: August 30, 2017
  2. Accepted: January 19, 2018
  3. Accepted Manuscript published: February 2, 2018 (version 1)
  4. Version of Record published: February 14, 2018 (version 2)

Copyright

© 2018, Steck 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. Kathrin Steck
  2. Samuel J Walker
  3. Pavel M Itskov
  4. Celia Baltazar
  5. José-Maria Moreira
  6. Carlos Ribeiro
(2018)
Internal amino acid state modulates yeast taste neurons to support protein homeostasis in Drosophila
eLife 7:e31625.
https://doi.org/10.7554/eLife.31625

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https://doi.org/10.7554/eLife.31625

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