Beneficial microorganisms associated with animals derive their nutritional requirements entirely from the animal host, but the impact of these microorganisms on host metabolism is largely unknown. The focus of this study was the experimentally tractable tripartite symbiosis between the pea aphid Acyrthosiphon pisum, its obligate intracellular bacterial symbiont Buchnera, and the facultative bacterium Hamiltonella which is localized primarily to the aphid hemolymph (blood). Metabolome experiments on, first, multiple aphid genotypes that naturally bear or lack Hamiltonella and, second, one aphid genotype from which Hamiltonella was experimentally eliminated revealed no significant effects of Hamiltonella on aphid metabolite profiles, indicating that Hamiltonella does not cause major reconfiguration of host metabolism. However, the titer of just one metabolite, 5-aminoimidazole-4-carboxamide ribonucleotide (AICAR), displayed near-significant enrichment in Hamiltonella-positive aphids in both metabolome experiments. AICAR is a by-product of biosynthesis of the essential amino acid histidine in Buchnera and, hence, an index of histidine biosynthetic rates, suggesting that Buchnera-mediated histidine production is elevated in Hamiltonella-bearing aphids. Consistent with this prediction, aphids fed on [¹³C]histidine yielded a significantly elevated ¹²C/¹³C ratio of histidine in Hamiltonella-bearing aphids, indicative of increased (∼25%) histidine synthesized de novo by Buchnera. However, in silico analysis predicted an increase of only 0.8% in Buchnera histidine synthesis in Hamiltonella-bearing aphids. We hypothesize that Hamiltonella imposes increased host demand for histidine, possibly for heightened immune-related functions. These results demonstrate that facultative bacteria can alter the dynamics of host metabolic interactions with co-occurring microorganisms, even when the overall metabolic homeostasis of the host is not substantially perturbed.

中文翻译：

---

兼性细菌对专性昆虫-细菌共生的代谢功能的影响。

与动物有关的有益微生物完全从动物宿主获得其营养需求，但是这些微生物对宿主代谢的影响很大程度上未知。这项研究的重点是豌豆蚜虫蚜虫，其专性细胞内细菌共生菌Buchnera和兼性细菌汉密尔顿菌之间的实验上易处理的三方共生，后者主要定位于蚜虫血淋巴（血）。代谢组学实验中，首先是自然携带或缺乏汉密尔顿杆菌的多种蚜虫基因型，其次是通过实验消除汉密尔顿杆菌的一种蚜虫基因型，未发现汉密尔顿杆菌在蚜虫代谢产物上的分布图，表明汉密尔顿杆菌不会引起宿主代谢的重大重构。然而，在两种代谢组实验中，仅一种代谢物5-氨基咪唑-4-羧酰胺核糖核苷酸（AICAR）的滴度显示了汉密尔顿氏菌阳性蚜虫的近乎显着的富集。AICAR是布氏杆菌中必需氨基酸组氨酸的生物合成的副产物，因此是组氨酸生物合成速率的指数，这表明在含汉密尔顿氏菌的蚜虫中布氏杆菌介导的组氨酸产量增加。与该预测一致，以[ ¹³ C]组氨酸为食的蚜虫的产量显着升高¹² C / ¹³中的组氨酸的C比Hamiltonella-轴承蚜虫，指示增加（〜25％）的组氨酸合成从头由鬼羽箭属。然而，计算机分析预测在含汉密尔顿杆菌的蚜虫中布氏杆菌组氨酸合成仅增加0.8％。我们假设汉密尔顿杆菌对组氨酸的宿主需求增加，可能是为了增强免疫相关功能。这些结果表明，兼性细菌可以改变宿主与共生微生物的代谢相互作用的动力学，即使基本上不干扰宿主的总体代谢稳态。