Yeast smell underpins partnership with fruit flies

Yeast produce fruity aromas that lure fruit flies to dinner. In return, the flies disperse the otherwise sedentary fungi, a new study suggests.

A gene called ATF1 allows Saccharomyces cerevisiae, also known as baker’s yeast or brewer’s yeast, to attract fruit flies, researchers demonstrate in the Oct. 23 Cell Reports.

The discovery puts the genetics and molecular biology of two commonly used laboratory organisms into ecological context, says Matthew Goddard, an evolutionary biologist at the University of Auckland in New Zealand. Goddard’s group previously found that wild fruit flies carry S. cerevisiae. The new work helps explain the genetics underlying that interaction, he says.

What was once thought to be a useless gene might be a lynchpin of a mutually beneficial relationship between yeast and flies, similar to that of flowers that produce scent to attract pollinator insects, says Bill Hansson, an evolutionary neuroethologist at the Max Planck Institute for Chemical Ecology in Jena, Germany.

Scientists have long known that yeast make aromatic acetate esters, which give beers and wines their distinctive bouquets. What they haven’t understood is why the fungi bother producing such energetically expensive molecules. Yeast that lack the ATF1 gene, which encodes an enzyme that produces the fruity aroma chemicals, grow just fine in the laboratory, says geneticist Kevin Verstrepen of Katholieke Universiteit Leuven and VIB, a research institute also in Leuven, Belgium.

“By studying these things as monocultures in a sterile environment we miss a lot of interesting behaviors,” he says.

Verstrepen got his first inkling about what the smelly stuff might be good for about 15 years ago when he left flasks of yeast sitting on his laboratory bench over a weekend. “It turned out I was doing an experiment without even knowing it,” he says.

When he came in on Monday morning, Verstrepen found that Drosophila melanogaster fruit flies from a neighboring lab had invaded his flasks. A flask containing a normal strain of lab yeast had attracted two fruit flies. Another flask held mutant yeast that pump out more of the acetate esters than usual. Fifty fruit flies had flocked to it. The final flask contained a mutant strain of yeast lacking ATF1. It lured zero flies. The accidental experiment intrigued Verstrepen, but he didn’t follow up on the observation until just a few years ago.

That’s when Verstrepen and neuroscientist Emre Yaksi of Neuro-Electronics Research Flanders, a nonprofit also in Leuven, talked over a beer about the observation. Yaksi studies chemical senses, such as taste and smell, in fruit flies and zebrafish. The two researchers decided to team up to see if yeast aromas really do attract flies and if so, why that would benefit yeast.

The researchers streamed air over an aromatic strain of yeast from a vineyard and a mutant strain that can’t make the strong-smelling compounds into opposite corners of a four-cornered plastic box. Fruit flies stampeded toward the fruity-smelling yeast but largely ignored the mutants. When the researchers wafted three acetate esters into the arena in the odorless yeast’s corner, more flies than before headed toward the mutants’ corner. That finding indicated that the esters are a component that attracts the flies.

It’s clear what the fruit flies get from being able to sniff out yeast: lunch. The flies chow down on yeast and get protein in their diet. Less obvious was why yeast would lure flies to the table. To find out, the researchers tagged aromatic and odorless mutant yeast with different colors of fluorescent proteins. They next placed a million cells of each strain on a petri dish. Fruit flies roamed the plates overnight in complete darkness.

Yeast that made the aromatic compounds were transported around the plate four times as often as the scentless mutants were, the researchers found. The finding indicates that yeast are trading a meal for a ride aboard a fruit fly to a new location. In the wild, yeast probably piggyback aboard flies as they visit ripening and rotting fruit.

Studies like this one that consider more than one organism at a time may help scientists discover the purpose of a large number of genes with no currently known function, Hansson says. And Tadashi Fukami, an ecologist at Stanford University, agrees. The study, he says, is an example of “melding, where ecology and molecular biology are being reunited and playing complementary roles.”