The boom and bust of the aphid’s essential amino acid metabolism across nymphal development

Within long-term symbioses, animals integrate their physiology and development with their symbiont. In a model nutritional mutualism, aphids harbor the endosymbiont, Buchnera, within specialized bacteriocyte cells. Buchnera synthesizes essential amino acids (EAAs) and vitamins for their host, which are lacking from the aphid’s plant sap diet. It is unclear if the aphid host differentially expresses aphid EAA metabolism pathways and genes that collaborate with Buchnera for the production of EAA and vitamins throughout nymphal development when feeding on plants. It is also unclear if aphid bacteriocytes are differentially methylated throughout aphid development as DNA methylation may play a role in gene regulation. By analyzing aphid gene expression, we determined that the bacteriocyte is metabolically more active in metabolizing Buchnera’s EAAs and vitamins early in nymphal development compared to intermediate or later immature and adult lifestages. The largest changes in aphid bacteriocyte gene expression, especially for aphid genes that collaborate with Buchnera, occurred during the 3rd to 4th instar transition. During this transition, there is a huge shift in the bacteriocyte from a high energy “nutrient-consuming state” to a “recovery and growth state” where patterning and signaling genes and pathways are upregulated and differentially methylated, and de novo methylation is reduced as evidenced by homogenous DNA methylation profiles after the 2nd instar. Moreover, bacteriocyte number increased and Buchnera’s titer decreased throughout aphid nymphal development. These data suggest in combination that bacteriocytes of older nymphal and adult lifestages depend less on the nutritional symbiosis compared to early nymphal lifestages.