In metabolizing spruce bark, insect’s fungal partners release volatile compounds that bark beetles detect through specialized olfactory sensory neurons – ScienceDaily

In a new study in the journal PLOS Biology, An international research team led by researchers from the Max Planck Institute for Chemical Ecology demonstrates that the European spruce bark beetle Ips typographus uses volatile fungal metabolites of plant defenses as important chemical signals for its attack on spruce. The researchers also show that the insects have olfactory sensory neurons that are specialized to detect these volatile compounds. The metabolites of the fungi probably give the beetles important clues about the presence of beneficial fungi, the defensive status of the trees, and the population density of their conspecifics. The study underscores the importance of chemical communication in maintaining the symbiosis between bark beetles and their fungal partners.

The mass outbreaks of bark beetles observed in recent years have caused alarming forest damage throughout Germany. As reported by the Federal Statistical Office in July 2022, more than 80% of the trees that had to be felled in the previous year were damaged by insects. The felling of damaged wood due to insect damage amounted to over 40 million solid cubic metres. One of the main pests is the European spruce beetle Ips typographus. In the Thuringian Forest and in the Harz Mountains, for example, the beetle, which was only a few millimeters in size, encountered spruce monocultures that had already been weakened by high temperatures and prolonged periods of drought, which facilitated the spread of the pest and led to the death of huge forest stands within a short period of time.

Researchers already know that chemical communication plays an important role in bark beetle mass attacks. Beetles first look for a suitable tree and then release so-called aggregation pheromones. These pheromones lure nearby conspecifics into a mass attack that overcomes the tree’s defences. Spruces whose defenses have already been weakened by stress are more easily overcome.

Bark beetles like the smell of their symbiotic fungi

Spruce bark beetles need fungal allies to successfully reproduce in the trees. The fungi are ectosymbionts, symbiotic partners that live outside of the beetles. Each new generation of bugs must find their symbiotic fungi and carry them to a new host tree.

In a new study, an international team of researchers led by Dineshkumar Kandasamy (now at Lund University, Sweden) and Jonathan Gershenzon from the Max Planck Institute for Chemical Ecology in Jena, Germany, report that the European spruce bark beetle can find its fungal partners on the volatile chemical compounds that the fungi release when breaking down spruce resin components. “We have already shown that bark beetles are attracted to their fungal partners when cultivated on standard fungal growth medium. Now we wanted to know what would happen if we grew mushrooms on a more natural medium with powdered spruce bark. Now, would bugs be attracted to fungi? If so, which chemical compounds would be responsible for the attraction and where do these chemicals come from?” First author Dineshkumar Kandasamy explains the initial questions of the study.

Fungi convert the chemical defenses in the spruce into attractants for the beetles

European spruce bark beetles are associated with fungal partners of different genera. The mushroom Grosmannia penicillata grew particularly well on the spruce bark medium and produced more volatile compounds than most other fungi tested. Therefore, the researchers focused their investigations on this fungus. The researchers set up special test fields where they could test whether the beetles were attracted to volatile compounds given off by the fungi.

“We first found that when growing fungi on medium containing spruce bark powder, European spruce bark beetles are attracted to the volatiles emitted by their associated fungi. However, we have also shown that fungi can convert terpene compounds from spruce resin into their oxygenated derivatives, and that some of these fungal-produced metabolites are particularly attractive to bark beetles. The general conclusion is that these volatiles serve as chemical signals that keep the symbiosis between bark beetles and their associated fungi going,” says Dineshkumar Kandasamy.

The researchers found that pathogenic fungi that harm the beetles can also metabolize spruce resin compounds. However, unlike the metabolites of the symbiotic fungi, the resulting derivatives are not attractive to bark beetles. Bark beetles can therefore use their sense of smell to distinguish whether the fungi present in the tree are good or bad for them. The scientists were particularly surprised when the behavioral observations showed that fungal partners not only attracted the beetles, but also stimulated them to tunnel.

Bark beetles have olfactory cells in their antennae that are geared towards sensing volatile compounds in fungal metabolism

Electrophysiological studies of the beetles’ odor perception provided further evidence that fungal metabolites make spruce trees already infested with fungi even more attractive to bark beetles. The reaction of individual olfactory sensillae on the beetle antennae to different smells was tested. The researchers were able to show that the bark beetles have specific olfactory neurons, which are housed in sensilla and are specialized in recognizing oxygen-rich monoterpenes that are released by the fungi.

“By increasing the bark beetle’s attraction to certain trees, fungal volatile compounds could increase the intensity and success of mass attacks. Fungi, which metabolize resinous compounds originally produced by the tree as a defense, could provide clues as to which fungi are virulent and good ones for the beetle.” could be partners,” says Jonathan Gershenzon.

Findings from this new study could help improve bark beetle outbreak control. One of the most common strategies used to combat these pests is pheromone traps, but these have not been effective in preventing new outbreaks. The researchers are therefore now examining whether these odor traps can be optimized by adding oxygen-containing monoterpenes from the fungal metabolism. An important goal of the research team is to learn more about the metabolism of the spruce resin compounds in the fungi and to find out whether this can be a detoxification reaction for the fungus or for the beetle.

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