Link between Energy Investment in Biosynthesis and Proteostasis: Testing the Cost–Quality Hypothesis in Insects

SIMPLE SUMMARY: The energy cost for synthesizing bio-tissue varies greatly among different species. We hypothesize that high energy cost stems from maintaining the protein homeostasis (proteostasis), including the cost of unfolding, degrading, and resynthesizing the proteins that have errors; as such, a large amount of synthesized protein does not contribute to growth. Our hypothesis predicts that the species with high energy cost have better cellular viability under stress due to better proteostasis, higher proteasome activities that break down proteins, and slower growth for a given amount of RNA that synthesizes proteins. We tested the hypothesis on two insect species, painted lady caterpillar and Turkestan cockroach nymph, the former’s biosynthetic energy cost being 20 times lower than the latter. The results support our hypothesis. ABSTRACT: The energy requirement for biosynthesis plays an important role in an organism’s life history, as it determines growth rate, and tradeoffs with the investment in somatic maintenance. This energetic trait is different between painted lady (Vanessa cardui) and Turkestan cockroach (Blatta lateralis) due to the different life histories. Butterfly caterpillars (holometabolous) grow 30-fold faster, and the energy cost of biosynthesis is 20 times cheaper, compared to cockroach nymphs (hemimetabolous). We hypothesize that physiologically the difference in the energy cost is partially attributed to the differences in protein retention and turnover rate: Species with higher energy cost may have a lower tolerance to errors in newly synthesized protein. Newly synthesized proteins with errors are quickly unfolded and refolded, and/or degraded and resynthesized via the proteasomal system. Thus, much protein output may be given over to replacement of the degraded new proteins, so the overall energy cost on biosynthesis is high. Consequently, the species with a higher energy cost for biosyntheses has better proteostasis and cellular resistance to stress. Our study found that, compared to painted lady caterpillars, the midgut tissue of cockroach nymphs has better cellular viability under oxidative stresses, higher activities of proteasome 20S, and a higher RNA/growth ratio, supporting our hypothesis. This comparative study offers a departure point for better understanding life history tradeoffs between somatic maintenance and biosynthesis.