An invasive beetle–fungus complex is maintained by fungal nutritional-compensation mediated by bacterial volatiles

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.

Symbiotic microbes aid host adaptation by metabolizing a deterrent host pine carbohydrate d -pinitol in a beetle-fungus invasive complex

“…Supplementation of D-pinitol promotes the growth of RTB's mutualistic partner L. procerum and symbiotic bacteria. Because of the poor nutritional condition in pine phloem, utilization of D-pinitol by L. procerum and symbiotic bacteria also alleviates the nutrient competition between RTB and associated microbes by leaving higher amounts of other nutrients, such as D-glucose, for RTB (34). In addition, various species of the Erwinia genus have been known as phytopathogens causing soft rots, bacterial wilt, and fire blight disease (53)(54)(55).…”

“…Unexpectedly, given its medicinal value, the degradation mechanism of d -pinitol is still unknown. Our prior studies found that L. procerum can use d -pinitol as a carbon source for growth ( 34 , 35 ), and RTB-associated bacteria ( Serratia liquefaciens B310, Rahnella aquatilis B301, and Pseudomonas sp. 7 B321) produced the bacterial volatile ammonia that accelerates d -pinitol utilization of L. procerum ( 34 , 35 ).…”

Characterization of Antennal Chemosensilla and Associated Chemosensory Genes in the Orange Spiny Whitefly, Aleurocanthus spiniferus (Quaintanca)

“…Transcription levels of these chemosensory genes were normalized by reference gene RPS28 ( Kang et al, 2017a ; Kong et al, 2021 ). Heatmaps of chemosensory genes were constructed by pheatmap in R 4.0.4 as Liu et al (2020) reported. Differences of selected chemosensory genes between male and female were subjected to Student’s t -test ( P < 0.05), while one-way analysis of variance (ANOVA) followed by separation of means with the Fisher’s protected least significant difference (LSD) test ( P < 0.05) was used for the difference among the different developmental stages.…”

Seasonal Shifts in Cold Tolerance and the Composition of the Gut Microbiome of Dendroctonus valens LeConte Occur Concurrently

“…In recent years, alongside the distribution of pine forest, RTB has spread to more northern regions of China, such as Liaoning province and the Inner Mongolia Autonomous Region [17][18][19]. Due to the severity of the RTB outbreak in China, various aspects of the invasion dynamics of this insect have been studied [14], including its ecology [20] and yeast associates [15], the bioactivities of microorganisms against host defensive monoterpenes [21], the survival of RTB and its adaptability to a climate warming scenario [22], and the diversity of fungi associated with the insect [23][24][25].…”