Journal Article

A gut microbial factor modulates locomotor behaviour in Drosophila

Argade, Sulabha, Mazmanian, Sarkis K., Marka, Szabolcs, Bartos, Imre, Schretter, Catherine E., Vielmetter, Jost, Marka, Zsuzsa

2018

Overview

While research into the biology of animal behaviour has primarily focused on the central nervous system, cues from peripheral tissues and the environment have been implicated in brain development and function 1 . There is emerging evidence that bidirectional communication between the gut and the brain affects behaviours including anxiety, cognition, nociception and social interaction 1 – 9 . Coordinated locomotor behaviour is critical for the survival and propagation of animals, and is regulated by internal and external sensory inputs 10 , 11 . However, little is known about how the gut microbiome influences host locomotion, or the molecular and cellular mechanisms involved. Here we report that germ-free status or antibiotic treatment results in hyperactive locomotor behaviour in the fruit fly Drosophila melanogaster . Increased walking speed and daily activity in the absence of a gut microbiome are rescued by mono-colonization with specific bacteria, including the fly commensal Lactobacillus brevis . The bacterial enzyme xylose isomerase from L. brevis recapitulates the locomotor effects of microbial colonization by modulating sugar metabolism in flies. Notably, thermogenetic activation of octopaminergic neurons or exogenous administration of octopamine, the invertebrate counterpart of noradrenaline, abrogates the effects of xylose isomerase on Drosophila locomotion. These findings reveal a previously unappreciated role for the gut microbiome in modulating locomotion, and identify octopaminergic neurons as mediators of peripheral microbial cues that regulate motor behaviour in animals. Female Drosophila that lack a microbiota are hyperactive, and xylose isomerase from Lactobacillus brevis is sufficient to reverse this effect.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/326/2565/2134 / 631/378/2632 / 631/378/3920 / 64/24 / Aldose-Ketose Isomerases - metabolism / Animal behavior / Animal locomotion / Animals / Anti-Bacterial Agents - pharmacology / Antibiotics / Anxiety / Bacteria / Brain / Carbohydrate metabolism / Carbohydrate Metabolism - drug effects / Central nervous system / Cognition / Colonization / Drosophila / Drosophila melanogaster / Drosophila melanogaster - drug effects / Drosophila melanogaster - metabolism / Drosophila melanogaster - microbiology / Drosophila melanogaster - physiology / Enzymes / Female / Fruit flies / Fruit flies (Tephritidae) / Gastrointestinal Microbiome - drug effects / Gastrointestinal Microbiome - physiology / Germ-Free Life / Germfree / Glucose metabolism / Homeostasis / Humanities and Social Sciences / Hyperactivity / Insects / Intestinal microflora / Lactobacillus brevis / Lactobacillus brevis - enzymology / Lactobacillus brevis - isolation & purification / Lactobacillus brevis - metabolism / Letter / Locomotion / Locomotion - drug effects / Locomotion - physiology / Metabolism / Microbiomes / Microbiota (Symbiotic organisms) / Microorganisms / Monosaccharides / Motor Activity - drug effects / Motor Activity - physiology / multidisciplinary / Nervous system / Neural Pathways / Neurons / Neurons - drug effects / Neurons - metabolism / Noradrenaline / Norepinephrine / Observations / Octopamine / Octopamine - metabolism / Octopamine - pharmacology / Pain perception / Phenols (Class of compounds) / Physiological aspects / Physiology / Science / Science (multidisciplinary) / Sleep / Social behavior / Social interactions / Symbiosis / Walking / Xylose / Xylose isomerase