Abstract
Mutualisms between symbiotic microbes and animals have been well documented, and nutritional relationships provide the foundation for maintaining beneficial associations. The well-studied mutualism between bark beetles and their fungi has become a classic model system in the study of symbioses. Despite the nutritional competition between bark beetles and beneficial fungi in the same niche due to poor nutritional feeding substrates, bark beetles still maintain mutualistic associations with beneficial fungi over time. The mechanism behind this phenomenon, however, remains largely unknown. Here, we demonstrated the bark beetle Dendroctonus valens LeConte relies on the symbiotic bacterial volatile ammonia, as a nitrogen source, to regulate carbohydrate metabolism of its mutualistic fungus Leptographium procerum to alleviate nutritional competition, thereby maintaining the stability of the bark beetle–fungus mutualism. Ammonia significantly reduces competition of L. procerum for carbon resources for D. valens larval growth and increases fungal growth. Using stable isotope analysis, we show the fungus breakdown of phloem starch into d-glucose by switching on amylase genes only in the presence of ammonia. Deletion of amylase genes interferes with the conversion of starch to glucose. The acceleration of carbohydrate consumption and the conversion of starch into glucose benefit this invasive beetle–fungus complex. The nutrient consumption–compensation strategy mediated by tripartite beetle–fungus–bacterium aids the maintenance of this invasive mutualism under limited nutritional conditions, exacerbating its invasiveness with this competitive nutritional edge.
Highlights
These authors contributed : Fanghua Liu, Jacob D
Our previous studies have shown that D. valens–L. procerum formed a mutualistic beetle–fungus invasive complex under the nutrient-poor bark, and this mutualism is consistently maintained for multiple generations [55]
We propose that D. valens maintains mutualistic associations with the beneficial symbiont L. procerum under poor nutrition with the symbiotic bacterial volatile regulating the mutualistic fungus’ carbohydrate metabolism
Summary
L. procerum is the most frequently isolated species from RTB and forms a tightly mutualistic beetle–fungus invasive complex, thereby contributing to RTB’s successful invasiveness in China [17, 42, 44] This invasive complex faces a severe challenge because the phloem that they consume is nutritionally poor (containing nitrogen-limited sources, recalcitrant carbohydrate sources, and plant defensive compounds) [9, 37]. Results showed that the associated bacterial volatile ammonia, as a nitrogen source, regulates the mutualistic fungus L. procerum’s monosaccharide consumption and starch metabolism pathway that optimizes both the mutualistic fungus’ growth and larval development of RTB. We speculated that this is a strategy that helps maintain mutualistic associations with beneficial symbionts for insects in substrates with limited nutrition
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