A Conserved Dedicated Olfactory Circuit for Detecting Harmful Microbes in Drosophila

• Published in: Cell 2012-12, Vol.151 (6), p.1345-1357
• Main Authors: Stensmyr, Marcus C., Dweck, Hany K.M., Farhan, Abu, Ibba, Irene, Strutz, Antonia, Mukunda, Latha, Linz, Jeanine, Grabe, Veit, Steck, Kathrin, Lavista-Llanos, Sofia, Wicher, Dieter, Sachse, Silke, Knaden, Markus, Becher, Paul G., Seki, Yoichi, Hansson, Bill S.
• Format: Article
• Language: English
• Subjects: Animals; Bacteria - chemistry; breeding sites; Chemoreceptor Cells - metabolism; chemotaxis; Drosophila - physiology; Drosophila melanogaster; Drosophila melanogaster - physiology; Feeding Behavior; Female; Fungi - chemistry; geosmin; Male; microbes; Naphthols - chemistry; odor compounds; Olfactory Pathways; olfactory receptors; Oviposition; Receptors, Odorant - metabolism; sensory neurons; Sensory Receptor Cells - physiology; toxicity; yeasts; Zoologi; Zoology
• ISSN: 0092-8674; 1097-4172; 1097-4172
• DOI: 10.1016/j.cell.2012.09.046

Flies, like all animals, need to find suitable and safe food. Because the principal food source for Drosophila melanogaster is yeast growing on fermenting fruit, flies need to distinguish fruit with safe yeast from yeast covered with toxic microbes. We identify a functionally segregated olfactory circuit in flies that is activated exclusively by geosmin. This microbial odorant constitutes an ecologically relevant stimulus that alerts flies to the presence of harmful microbes. Geosmin activates only a single class of sensory neurons expressing the olfactory receptor Or56a. These neurons target the DA2 glomerulus and connect to projection neurons that respond exclusively to geosmin. Activation of DA2 is sufficient and necessary for aversion, overrides input from other olfactory pathways, and inhibits positive chemotaxis, oviposition, and feeding. The geosmin detection system is a conserved feature in the genus Drosophila that provides flies with a sensitive, specific means of identifying unsuitable feeding and breeding sites. [Display omitted] [Display omitted] ► Geosmin, the odor of mold, activates only olfactory sensory neurons expressing Or56a ► These neurons connect to projection neurons that respond exclusively to geosmin ► This circuit confers innate avoidance and, upon activation, overrides attraction ► This pathway is used by flies to detect harmful microbes that produce geosmin A neuronal circuit that detects a volatile chemical released by toxic mold has been mapped in fly brain. Activation of this evolutionarily conserved circuit overrides a number of innate behaviors such as attraction to other odors and egg laying on substrates, revealing the underlying mechanisms of hard-wired and selectively advantageous avoidance of harmful bacteria in the environment.