State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, 100101, Beijing, China.
CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, 100049, Beijing, China.
ISME J. 2020 Nov;14(11):2829-2842. doi: 10.1038/s41396-020-00740-w. Epub 2020 Aug 19.
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.
共生微生物与动物之间的互惠共生关系已有大量文献记载，营养关系为维持有益关联提供了基础。在研究共生关系时，研究得很好的树皮甲虫与其真菌之间的互惠共生关系已成为一个经典模式系统。尽管由于营养贫瘠的饲料基质，树皮甲虫和有益真菌之间存在营养竞争，但随着时间的推移，树皮甲虫仍与有益真菌保持着互惠共生关系。然而，这种现象背后的机制在很大程度上仍然未知。在这里，我们证明了树皮甲虫 Dendroctonus valens LeConte 依赖共生细菌挥发性氨作为氮源，调节其共生真菌 Leptographium procerum 的碳水化合物代谢，以减轻营养竞争，从而维持树皮甲虫-真菌共生体的稳定性。氨显著降低了 L. procerum 对 D. valens 幼虫生长所需碳资源的竞争，并增加了真菌的生长。通过稳定同位素分析，我们表明，在存在氨的情况下，真菌通过开启淀粉酶基因将韧皮部淀粉分解为 D-葡萄糖。淀粉酶基因的缺失会干扰淀粉向葡萄糖的转化。碳水化合物消耗的加速和淀粉向葡萄糖的转化有利于这种入侵性甲虫-真菌复合体。由三方参与的甲虫-真菌-细菌的营养消耗补偿策略有助于在有限的营养条件下维持这种入侵性互惠共生关系，通过这种竞争营养优势加剧了其入侵性。
