Université Lyon, INRAE, INSA-Lyon, BF2I, UMR 203, Villeurbanne, France.
Laboratoire de Biométrie et Biologie Evolutive, UMR5558, Université Lyon 1, Université Lyon, Villeurbanne, France.
mBio. 2023 Apr 25;14(2):e0333322. doi: 10.1128/mbio.03333-22. Epub 2023 Feb 13.
Nutritional symbioses between insects and intracellular bacteria (endosymbionts) are a major force of adaptation, allowing animals to colonize nutrient-poor ecological niches. Many beetles feeding on tyrosine-poor substrates rely on a surplus of aromatic amino acids produced by bacterial endosymbionts. This surplus of aromatic amino acids is crucial for the biosynthesis of a thick exoskeleton, the cuticle, which is made of a matrix of chitin with proteins and pigments built from tyrosine-derived molecules, providing an important defensive barrier against biotic and abiotic stress. Other endosymbiont-related advantages for beetles include faster development and improved fecundity. The association between Sitophilus oryzae and the Sodalis pierantonius endosymbiont represents a unique case study among beetles: endosymbionts undergo an exponential proliferation in young adults concomitant with the cuticle tanning, and then they are fully eliminated. While endosymbiont clearance, as well as total endosymbiont titer, are host-controlled processes, the mechanism triggering endosymbiont exponential proliferation remains poorly understood. Here, we show that endosymbiont exponential proliferation relies on host carbohydrate intake, unlike the total endosymbiont titer or the endosymbiont clearance, which are under host genetic control. Remarkably, insect fecundity was preserved, and the cuticle tanning was achieved, even when endosymbiont exponential proliferation was experimentally blocked, except in the context of a severely unbalanced diet. Moreover, a high endosymbiont titer coupled with nutrient shortage dramatically impacted host survival, revealing possible environment-dependent disadvantages for the host, likely due to the high energy cost of exponentially proliferating endosymbionts. Beetles thriving on tyrosine-poor diet sources often develop mutualistic associations with endosymbionts able to synthesize aromatic amino acids. This surplus of aromatic amino acids is used to reinforce the insect's protective cuticle. An exceptional feature of the / interaction is the exponential increase in endosymbiotic titer observed in young adult insects, in concomitance with cuticle biosynthesis. Here, we show that host carbohydrate intake triggers endosymbiont exponential proliferation, even in conditions that lead to the detriment of the host survival. In addition, when hosts thrive on a balanced diet, endosymbiont proliferation is dispensable for several host fitness traits. The endosymbiont exponential proliferation is therefore dependent on the nutritional status of the host, and its consequences on host cuticle biosynthesis and survival depend on food quality and availability.
昆虫与细胞内细菌（内共生体）之间的营养共生是适应的主要力量，使动物能够在营养贫瘠的生态位中殖民。许多以酪氨酸含量低的基质为食的甲虫依赖于细菌内共生体产生的芳香族氨基酸过剩。这种芳香族氨基酸的过剩对于厚外骨骼的生物合成至关重要，外骨骼由几丁质基质与来自酪氨酸的分子构建的蛋白质和色素组成，为生物和非生物胁迫提供了重要的防御屏障。内共生体相关的其他优势包括甲虫更快的发育和更高的繁殖力。Sitophilus oryzae 与 Sodalis pierantonius 内共生体的关联代表了甲虫中的一个独特案例研究：内共生体在年轻成虫中经历指数增殖，伴随着角质层鞣制，然后被完全消除。虽然内共生体清除和总内共生体滴度是宿主控制的过程，但触发内共生体指数增殖的机制仍知之甚少。在这里，我们表明，与总内共生体滴度或内共生体清除不同，内共生体的指数增殖依赖于宿主的碳水化合物摄入，而内共生体清除和总内共生体滴度受宿主遗传控制。值得注意的是，即使实验性地阻断了内共生体的指数增殖，昆虫的繁殖力得以保持，角质层鞣制得以实现，除了在严重不平衡饮食的情况下。此外，高内共生体滴度加上营养短缺极大地影响了宿主的生存，这表明宿主可能存在环境依赖的劣势，这可能是由于指数增殖的内共生体的高能量成本。在酪氨酸含量低的饮食源上茁壮成长的甲虫通常与能够合成芳香族氨基酸的内共生体形成互利共生关系。这种芳香族氨基酸的过剩被用来增强昆虫的保护性外骨骼。/ 相互作用的一个特殊特征是在年轻成虫中观察到内共生体滴度的指数增加，与角质层生物合成同时发生。在这里，我们表明，即使在宿主生存受到损害的情况下，宿主的碳水化合物摄入也会触发内共生体的指数增殖。此外，当宿主在平衡饮食中茁壮成长时，内共生体的增殖对于宿主的几个适应特征是可有可无的。因此，内共生体的指数增殖依赖于宿主的营养状况，其对宿主角质层生物合成和生存的影响取决于食物的质量和可获得性。
