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Journal Article
A neurotransmitter produced by gut bacteria modulates host sensory behaviour
2020
Overview
Animals coexist in commensal, pathogenic or mutualistic relationships with complex communities of diverse organisms, including microorganisms
1
. Some bacteria produce bioactive neurotransmitters that have previously been proposed to modulate nervous system activity and behaviours of their hosts
2
,
3
. However, the mechanistic basis of this microbiota–brain signalling and its physiological relevance are largely unknown. Here we show that in
Caenorhabditis elegans
, the neuromodulator tyramine produced by commensal
Providencia
bacteria, which colonize the gut, bypasses the requirement for host tyramine biosynthesis and manipulates a host sensory decision. Bacterially produced tyramine is probably converted to octopamine by the host tyramine β-hydroxylase enzyme. Octopamine, in turn, targets the OCTR-1 octopamine receptor on ASH nociceptive neurons to modulate an aversive olfactory response. We identify the genes that are required for tyramine biosynthesis in
Providencia
, and show that these genes are necessary for the modulation of host behaviour. We further find that
C. elegans
colonized by
Providencia
preferentially select these bacteria in food choice assays, and that this selection bias requires bacterially produced tyramine and host octopamine signalling. Our results demonstrate that a neurotransmitter produced by gut bacteria mimics the functions of the cognate host molecule to override host control of a sensory decision, and thereby promotes fitness of both the host and the microorganism.
A neuromodulator produced by commensal
Providencia
bacteria that colonize the gut of
Caenorhabditis elegans
mimics the functions of the cognate host molecule to manipulate a sensory decision of the host.
Publisher
Nature Publishing Group UK,Nature Publishing Group
Subject
/ 64/11
/ Animals
/ Avoidance Learning - drug effects
/ Bacteria
/ Behavior
/ Caenorhabditis elegans - drug effects
/ Caenorhabditis elegans - microbiology
/ Caenorhabditis elegans - physiology
/ Caenorhabditis elegans Proteins - genetics
/ Caenorhabditis elegans Proteins - metabolism
/ Feeding Behavior - physiology
/ Food
/ Gastrointestinal Microbiome - physiology
/ Genes
/ Humanities and Social Sciences
/ Microbiota (Symbiotic organisms)
/ Mutation
/ Neurotransmitter Agents - metabolism
/ Receptors, Biogenic Amine - metabolism
/ Receptors, G-Protein-Coupled - metabolism
/ Science
/ Sensory Receptor Cells - metabolism
/ Tyramine
/ Tyrosine Decarboxylase - deficiency
/ Tyrosine Decarboxylase - genetics
/ Worms
