Quantifying supply and demand in the pea aphid-Buchnera symbiosis reveals the metabolic Achilles’ heels of this interaction

Many herbivorous insects feed on unbalanced diets and rely on bacterial endosymbionts to meet all their nutritional needs. This is the case for the pea aphid (Acyrthosiphon pisum), a plant pest whose remarkable growth and reproductive capacities cannot be sustained by its sole nutritional resource, the plant phloem sap, and which relies on a symbiotic relationship maintained over millions of years with the intracellular bacterium Buchnera aphidicola for the biosynthesis of amino acids and vitamins. Exploiting original experimental data and metabolic reconstructions, we have built a quantitative genome-scale metabolic model of B. aphidicola and used it to quantify amino acid exchanges between the bacterium and its host. We found metabolites that can rewire pathways, influencing the balance between selfish (growth-focused) and mutualist (amino acid synthesis) behavior. Among the products synthesized by Buchnera, phenylalanine, tyrosine and leucine are the main matter sinks and consume more than 60 % of imported glucose and serine. Finally, we compared the predicted bacterial supply to the aphid demand in amino acids. We found that the pea aphid may efficiently regulate its symbiont population density depending on its metabolic requirements, but that embryos are quantitatively not self-sustaining, with embryonic bacteria supply falling short of demand by 50 %. Overall, our study highlights candidate compounds and pathways to target for destabilizing this symbiosis or predicting its resilience to environmental or nutritional perturbations.