Biosynthetic constraints on amino acid synthesis at the base of the food chain may determine their use in higher-order consumer genomes

Dietary nutrient composition is essential for shaping important fitness traits and behaviours. Many organisms are protein limited, and for Drosophila melanogaster this limitation manifests at the level of the single most limiting essential Amino Acid (AA) in the diet. The identity of this AA and its effects on female fecundity is readily predictable by a procedure called exome matching in which the sum of AAs encoded by a consumer's exome is used to predict the relative proportion of AAs required in its diet. However, the exome matching calculation does not weight AA contributions to the overall profile by protein size or expression. Here, we update the exome matching calculation to include these weightings. Surprisingly, although nearly half of the transcriptome is differentially expressed when comparing male and female flies, we found that creating transcriptome-weighted exome matched diets for each sex did not enhance their fecundity over that supported by exome matching alone. These data indicate that while organisms may require different amounts of dietary protein across conditions, the relative proportion of the constituent AAs remains constant. Interestingly, we also found that exome matched AA profiles are generally conserved across taxa and that the composition of these profiles might be explained by energetic and elemental limitations on microbial AA synthesis. Thus, it appears that ecological constraints amongst autotrophs shape the relative proportion of AAs that are available across trophic levels and that this constrains biomass composition. Author summaryThe amount and type of food that organisms consume shapes their fitness. Many species, including the fruitfly Drosophila melanogaster, suffer protein-limitation, which means they must evolve strategies to make the most of the protein they consume. We previously discovered that this protein limitations manifests at the level of individual amino acids for egg production in fruitflies.Here, we attempt to improve dietary amino acid proportions (protein quality) for male and female reproduction in the fruitfly. We do this by tailoring the fly's diet to contain amino acids in the proportions found in all the expressed proteins of either male or female Drosophila. In doing so, we discover that, despite functional differences between the sexes, their pattern of genome-encoded amino acid utilisation is remarkably conserved. In fact, this amino acid profile is also conserved in other species' genomes from bacteria to humans. We hypothesise that this conservation represents an evolutionary strategy for organisms to make the most of limited amounts of dietary protein.