How The Transition of Aphid Life Cycles Affect Endosymbiotic Bacteria

Abstract

How symbiotic bacteria coordinate and respond to their hosts during complex life cycle transitions is a fascinating and unresolved topic, particularly for organisms that exist solely in natural environments, where their intricate life cycles make laboratory cultivation extremely challenging. Complex life cycles are often associated with host alternation in aphids, especially in eriosomatine gall-forming aphids, which exhibit seven distinct morphs throughout their life cycle while shifting their host plants seasonally. Despite these dramatic changes, these aphids maintain the obligate symbiotic bacterium, Buchnera aphidicola, to enhance their nutritional status. The bacterial communities in our wild-derived samples were dominated by aphid symbionts, including Buchnera, Regiella inseticola, Wolbachia, Arsenophonus, and Serratia symbiotica. Buchnera and Regiella prevailed in Tetraneura akinire and Tetraneura sorini, while Buchnera and Arsenophonus were more abundant in Eriosoma harunire. Our study, utilizing 16S rRNA metagenomic sequencing on the aphid Tetraneura akinire, demonstrates that Buchnera plays significant roles during most life cycle stages but is absent during the sexual male stage, where it is replaced by Regiella. Moreover, Buchnera densities exhibit significant variability across the aphids life cycles and are notably lower in gall generations. This result contradicts the previous hypothesis that galls provide superior nutrition compared to aphids in grassroot-feeding generations. In this study, we reveal the dynamics of symbiotic bacteria across the complex life cycles of three eriosomatine aphid species that form galls on the same Japanese elm tree, Ulmus davidiana var. japonica. Within the framework of tripartite symbiosis, the seemingly passive symbiotic bacteria adjust the hosts specific life stages and influence the changing host ecology in a cascading manner.