How Flies Avoid Rotten Food
December 7, 2012

When Good Food Goes Bad, Smart Flies Keep Their Distance

[ Watch the Video: Flies Sniff Out and Avoid Spoiled Food ]

April Flowers for - Your Universe Online

Eating spoiled food can be fatal as it allows bacterial pathogens to enter the digestive system. One of the main tasks of the sense of smell is to detect signs of decay, allowing us and other animals to avoid such food poisoning.

A new study, conducted by behavioral scientists and neurobiologists at the Max Planck Institute for Chemical Ecology, has decoded the neural mechanisms underlying an escape reflex in fruit flies (Drosophila) for the first time. This escape reflex is activated in order to avoid eating and laying eggs in food infected by toxic microorganisms.

As soon as the tiniest bit of geosmin — a substance released by bacteria and mold fungi toxic to the fly — is in the air, a super-sensitive and completely dedicated neural line, from olfactory receptor, via sensory neuron and primary brain neurons, is activated, overriding all other food odor signals regardless of how attractive they are on their own. Geosmin is a full stop signal for the flies that prevents them from eating and laying eggs in toxic food, a lot like when we open the refrigerator and smell last week's forgotten dinner.

In 2011, a shocking number of deaths in Germany were linked to fenugreek sprouts contaminated with EHEC (enterohaemorrhagic E. coli) bacteria revealed that it is crucial for every foraging organism to distinguish between fresh food and food that is infected with pathogenic microbes. Whether meats or vegetables, all foods are colonized by bacteria and other microbes. The numbers of microorganisms in the food varies with different degrees of freshness and storage conditions. The immune system can usually deal with these microorganisms, allowing the safe consumption of food as long as the decay hasn't gone too far. But when such pathogenic microbes have become dangerously high, what protects us and other animals?

Visual signs, in many cases, allow us to avoid rotten food. More directly, certain odors released by hazardous microbes and/or their activities tell us when foods should be discarded. The team wanted to understand what neural functions underlie such an avoidance or flight behavior by mapping the path from the odor molecule and the olfactory receptors into the brain to understand the animal's reaction.

The fruit fly Drosophila melanogaster and related species are genetically characterized, making them perfect study objects to answer such a question. Typically, the flies feed on yeasts growing on rotting fruit, making it imperative that they distinguish between "good" and "bad" microbes at this stage. The team showed that flies consuming pathogenic bacteria or fungi died very fast, and eggs deposited did not result in viable larvae.

Geosmin is an odor substance known to be produced by several fungi and bacteria and may trigger deterrent reactions. Quite familiar, geosmin is thought to be responsible for the strong scent of wet soils, especially after a drought. Highly sensitive to this odor, the human nose can detect it at concentrations as low as 0.1 parts per billion. The new study, published in the journal Cell, shows that Drosophila antennae are even more sensitive.

"When this compound is present in the air, even the most attractive food source becomes unattractive," said senior study author Bill Hansson of the Max Planck Institute for Chemical Ecology. "This is highly interesting, as it's seldom that single compounds have a direct behavioral effect and that they are active at extremely low concentrations as we observe here."

"We started with electrophysiological experiments and analyzed all olfactory sensory neurons on the fly antenna successively — more than thousand measurements," said lead study author Marcus Stensmyr.

Only a single neuron labeled "ab4B" responded to geosmin at this stage. These neurons carry a specific receptor (Or56a) which reacts exclusively to geosmin. The team was able to establish the specificity in both single neuron recordings linked to gas chromatography, testing more than 3,000 odors, and in experiments using cell cultures ectopically expressing the receptor.

Another interesting result was revealed when the team performed optical imaging of the Drosophila brain: from the approximately 50 glomeruli that constitute the antennal lobe, the olfactory center of the flies, only one, labeled DA2, was activated by geosmin. Other glomeruli that are involved in odor evoked aversion behavior were found in the same region as DA2.  When the team stimulated DA2, it activated a single type of a specific projection neuron (PN) conveying the message of geosmin presence to higher brain areas. Usually, PNs are more broadly tuned, providing a cross-glomerulus pattern for olfactory coding.

"However, this is different in the case of geosmin, Or56a, DA2 and the related PNs," said Hansson.

The stimulus is directly patched through from antennae to behavior in this circuit, the scientists say, without any detours. Previously, such patterns have only been observed in the responses to sex pheromones. This is the first time a fully dedicated neural pathway for an odor involved in feeding behavior has been revealed.

Using the recently established "Flywalk" system, where a single fly is placed into a small glass tube and different odors are applied to allow a computer / camera system to quantify behaviors, behavioral assays confirmed the nerve and brain measurements in the laboratory.

Not only does the geosmin stimulus, mediated through the neural line, cause the flies to stop or move away from the source of the odor, it overrides all simultaneously offered highly attractive odors, such as vinegar or fruit scents, at minute concentrations. This helps the fly avoid accidental consumption of pathogens by overriding even mixed smells. Odor mixtures are the rule, not the exception, in nature, making this a very important survival tool.

"It is obviously highly important for all organisms to stay away from spoiled food," concluded Stensmyr. "Detecting and avoiding food infested by bad microbes seems to be a ubiquitous phenomenon, where the nervous system has evolved to extreme degrees to make it work."