Department of Evolutionary Ecology, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University Mainz, Mainz 55128, Germany.
Department of Insect Symbiosis, Max-Planck-Institute for Chemical Ecology, Jena 07745, Germany.
Proc Natl Acad Sci U S A. 2023 Aug;120(31):e2302721120. doi: 10.1073/pnas.2302721120. Epub 2023 Jul 24.
Symbioses with microbes play a pivotal role in the evolutionary success of insects, and can lead to intimate host-symbiont associations. However, how the host maintains a stable symbiosis with its beneficial partners while keeping antagonistic microbes in check remains incompletely understood. Here, we uncover a mechanism by which a host protects its symbiont from the host's own broad-range antimicrobial defense during transmission. Beewolves, a group of solitary digger wasps (Hymenoptera: Crabronidae), provide their brood cells with symbiotic bacteria that are later transferred to the cocoon and protect the offspring from opportunistic pathogens by producing antibiotics. In the brood cell, however, the symbiont-containing secretion is exposed to a toxic burst of nitric oxide (NO) released by the beewolf egg, which effectively kills antagonistic microorganisms. How the symbiont survives this lethal NO burst remained unknown. Here, we report that upon NO exposure in vitro, the symbionts mount a global stress response, but this is insufficient to ensure survival at brood cell-level NO concentrations. Instead, in vivo bioassays demonstrate that the host's antennal gland secretion (AGS) surrounding the symbionts in the brood cell provides an effective diffusion barrier against NO. This physicochemical protection can be reconstituted in vitro by beewolf hydrocarbon extracts and synthetic hydrocarbons, indicating that the host-derived long-chain alkenes and alkanes in the AGS are responsible for shielding the symbionts from NO. Our results reveal how host adaptations can protect a symbiont from host-generated oxidative and nitrosative stress during transmission, thereby efficiently balancing pathogen defense and mutualism maintenance.
共生微生物在昆虫的进化成功中起着关键作用，并能导致亲密的宿主-共生体关联。然而，宿主如何在与有益伙伴保持稳定共生的同时，控制敌对微生物，仍然不完全清楚。在这里，我们揭示了一种宿主在传播过程中保护其共生体免受宿主广泛的抗菌防御的机制。蜜蜂，一群独居的挖掘黄蜂（膜翅目：Crabronidae），为其幼虫细胞提供共生细菌，这些细菌后来被转移到茧中，并通过产生抗生素来保护后代免受机会性病原体的侵害。然而，在幼虫细胞中，含有共生体的分泌物会暴露于蜜蜂卵释放的有毒一氧化氮（NO）爆发中，这有效地杀死了敌对的微生物。共生体如何在这种致命的 NO 爆发中存活下来仍然未知。在这里，我们报告说，在体外暴露于 NO 时，共生体会启动全局应激反应，但这不足以确保在幼虫细胞水平的 NO 浓度下存活。相反，体内生物测定表明，宿主的触角腺分泌物（AGS）围绕幼虫细胞中的共生体提供了一种有效的扩散屏障，防止 NO 进入。这种物理化学保护可以通过蜜蜂的碳氢化合物提取物和合成碳氢化合物在体外重建，表明宿主衍生的 AGS 中的长链烯烃和烷烃负责保护共生体免受 NO 的侵害。我们的研究结果揭示了宿主适应如何在传播过程中保护共生体免受宿主产生的氧化和硝化应激，从而有效地平衡病原体防御和共生维持。
