Biodiversity Research Centre, Earth and Life Institute, UCLouvain, Louvain-la-Neuve, Belgium.
Université de Lyon, INSA Lyon, INRAE, BF2I, UMR203, Villeurbanne, France.
Microbiol Spectr. 2022 Jun 29;10(3):e0045722. doi: 10.1128/spectrum.00457-22. Epub 2022 Jun 1.
Dependence on multiple nutritional symbionts that form a metabolic unit has evolved many times in insects. Although it has been postulated that host dependence on these metabolically interconnected symbionts is sustained by their high degree of anatomical integration (these symbionts are often housed in distinct symbiotic cells, the bacteriocytes, assembled into a common symbiotic organ, the bacteriome), the developmental aspects of such multipartner systems have received little attention. Aphids of the subfamilies Chaitophorinae and Lachninae typically harbor disymbiotic systems in which the metabolic capabilities of the ancient obligate symbiont Buchnera aphidicola are complemented by those of a more recently acquired nutritional symbiont, often belonging to the species Serratia symbiotica. Here, we used microscopy approaches to finely characterize the tissue tropism and infection dynamics of the disymbiotic system formed by B. aphidicola and S. symbiotica in the Norway maple aphid Periphyllus lyropictus (Chaitophorinae). Our observations show that, in this aphid, the co-obligate symbiont exhibits a dual lifestyle: intracellular by being housed in large syncytial bacteriocytes embedded between -containing bacteriocytes in a well-organized compartmentalization pattern, and extracellular by massively invading the digestive tract and other tissues during embryogenesis. This is the first reported case of an obligate aphid symbiont that is internalized in bacteriocytes but simultaneously adopts an extracellular lifestyle. This unusual infection pattern for an obligate insect symbiont suggests that some bacteriocyte-associated obligate symbionts, despite their integration into a cooperative partnership, still exhibit invasive behavior and escape strict compartmentalization in bacteriocytes. Multipartner nutritional endosymbioses have evolved many times in insects. In Chaitophorinae aphids, the eroded metabolic capabilities of the ancient obligate symbiont are complemented by those of more recently acquired symbionts. Here, we report the atypical case of the co-obligate symbiont associated with . This bacterium is compartmentalized into bacteriocytes nested into the ones harboring the more ancient symbiont , reflecting metabolic convergences between the two symbionts. At the same time, exhibits highly invasive behavior by colonizing various host tissues, including the digestive tract during embryogenesis. The discovery of this unusual phenotype for a co-obligate symbiont reveals a new face of multipartner nutritional endosymbiosis in insects. In particular, it shows that co-obligate symbionts can retain highly invasive traits and suggests that host dependence on these bacterial partners may evolve prior to their strict compartmentalization into specialized host structures.
昆虫中多次进化出依赖形成代谢单位的多种营养共生体。虽然有人假设，宿主对这些代谢上相互关联的共生体的依赖是由它们高度的解剖学整合维持的（这些共生体通常位于不同的共生细胞中，即菌细胞中，组装成一个共同的共生器官，即菌质体），但这种多伴侣系统的发育方面却很少受到关注。Chaitophorinae 和 Lachninae 亚科的蚜虫通常具有二相共生系统，其中古老的专性共生体 Buchnera aphidicola 的代谢能力被最近获得的营养共生体补充，这些共生体通常属于 Serratia symbiotica 种。在这里，我们使用显微镜方法精细地表征了在挪威枫蚜虫 Periphyllus lyropictus（Chaitophorinae）中由 Buchnera aphidicola 和 Serratia symbiotica 形成的二相共生系统的组织趋向性和感染动态。我们的观察表明，在这种蚜虫中，共生体 表现出双重生活方式：通过被包裹在大的合胞菌细胞中而成为细胞内共生体，这些合胞菌细胞嵌入在含有菌细胞的区域中，形成一种组织良好的分隔模式，并且在胚胎发生期间，通过大量入侵消化道和其他组织而成为细胞外共生体。这是首例报道的专性蚜虫共生体被内化到菌细胞中，但同时又采用细胞外生活方式的案例。这种对于专性昆虫共生体的不寻常感染模式表明，尽管一些菌细胞相关的专性共生体已经整合到合作关系中，但它们仍然表现出侵袭行为，并逃避菌细胞的严格分隔。多伴侣营养共生体在昆虫中多次进化。在 Chaitophorinae 蚜虫中，古老的专性共生体 Buchnera aphidicola 已经侵蚀的代谢能力被最近获得的共生体所补充。在这里，我们报告了与 共生的伴生共生体的非典型案例。这种细菌被分隔到菌细胞中，菌细胞嵌套在容纳更古老共生体的菌细胞中，反映了两种共生体之间的代谢趋同。同时，共生体 通过在胚胎发生期间殖民各种宿主组织，包括消化道，表现出高度的侵袭行为。这种共生体的不寻常表型的发现揭示了昆虫多伴侣营养共生体的一个新面貌。特别是，它表明伴生共生体可以保留高度侵袭的特征，并表明宿主对这些细菌伙伴的依赖可能在它们被严格分隔到专门的宿主结构之前就已经进化了。
