Serotonin deficiency from constitutive SKN-1 activation drives pathogen apathy

Nat Commun. 2024 Sep 16;15(1):8129. doi: 10.1038/s41467-024-52233-5.

Abstract

When an organism encounters a pathogen, the host innate immune system activates to defend against pathogen colonization and toxic xenobiotics produced. C. elegans employ multiple defense systems to ensure survival when exposed to Pseudomonas aeruginosa including activation of the cytoprotective transcription factor SKN-1/NRF2. Although wildtype C. elegans quickly learn to avoid pathogens, here we describe a peculiar apathy-like behavior towards PA14 in animals with constitutive activation of SKN-1, whereby animals choose not to leave and continue to feed on the pathogen even when a non-pathogenic and healthspan-promoting food option is available. Although lacking the urgency to escape the infectious environment, animals with constitutive SKN-1 activity are not oblivious to the presence of the pathogen and display the typical pathogen-induced intestinal distension and eventual demise. SKN-1 activation, specifically in neurons and intestinal tissues, orchestrates a unique transcriptional program which leads to defects in serotonin signaling that is required from both neurons and non-neuronal tissues. Serotonin depletion from SKN-1 activation limits pathogen defenses capacity, drives the pathogen-associated apathy behaviors and induces a synthetic sensitivity to selective serotonin reuptake inhibitors. Taken together, our work reveals interesting insights into how animals perceive environmental pathogens and subsequently alter behavior and cellular programs to promote survival.

MeSH terms

  • Animals
  • Apathy / physiology
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / immunology
  • Caenorhabditis elegans* / microbiology
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Host-Pathogen Interactions / immunology
  • Immunity, Innate
  • Neurons / metabolism
  • Pseudomonas Infections / immunology
  • Pseudomonas Infections / metabolism
  • Pseudomonas Infections / microbiology
  • Pseudomonas aeruginosa* / pathogenicity
  • Pseudomonas aeruginosa* / physiology
  • Selective Serotonin Reuptake Inhibitors / pharmacology
  • Serotonin* / metabolism
  • Signal Transduction
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • skn-1 protein, C elegans
  • Caenorhabditis elegans Proteins
  • Transcription Factors
  • Serotonin
  • DNA-Binding Proteins
  • Selective Serotonin Reuptake Inhibitors