Metabolic Cost of Protein Synthesis in Larvae of the Pacific Oyster (Crassostrea gigas) Is Fixed Across Genotype, Phenotype, and Environmental Temperature

Abstract

The energy made available through catabolism of specific biochemical reserves is constant using standard thermodynamic conversion equivalents (e.g., 24.0 J mg protein(-1)). In contrast, measurements reported for the energy cost of synthesis of specific biochemical constituents are highly variable. In this study, we measured the metabolic cost of protein synthesis and determined whether this cost was influenced by genotype, phenotype, or environment. We focused on larval stages of the Pacific oyster Crassostrea gigas, a species that offers several experimental advantages: availability of genetically pedigreed lines, manipulation of ploidy, and tractability of larval forms for in vivo studies of physiological processes. The cost of protein synthesis was measured in larvae of C. gigas for 1) multiple genotypes, 2) phenotypes with different growth rates, and 3) different environmental temperatures. For all treatments, the cost of protein synthesis was within a narrow range--near the theoretical minimum--with a fixed cost (mean ± one standard error, n = 21) of 2.1 ± 0.2 J (mg protein synthesized)(-1) We conclude that there is no genetic variation in the metabolic cost of protein synthesis, thereby simplifying bioenergetic models. Protein synthesis is a major component of larval metabolism in C. gigas, accounting for more than half the metabolic rate in diploid (59%) and triploid larvae (54%). These results provide measurements of metabolic cost of protein synthesis in larvae of C. gigas, an indicator species for impacts of ocean change, and provide a quantitative basis for evaluating the cost of resilience.

Biochemical bases of growth variation during development: A study of protein turnover in pedigreed families of bivalve larvae (Crassostrea gigas)

“…Rates of protein synthesis were determined using the methods developed for larvae of C. gigas by Lee et al (2016). A total of 114 protein synthesis assays (six time points per assay, Fig.…”

“…S1). The amount of total glycine (moles) incorporated into proteins was converted to the amount of proteins synthesized (grams), based on the mole-percent glycine in proteins for larvae of C. gigas (12 ±0.2%) and the average molecular mass of amino acids in proteins (126.6±0.2 g mol −1 , calculated from the amino acid composition of hydrolyzed protein) (Lee et al, 2016). For each analysis, protein synthesis rate was calculated from the slope of the linear regression describing the relationship between the amount of newly synthesized proteins and assay time ( Fig.…”

“…6B, shaded areas: 2355 µJ) (see Gnaiger, 1983, for general oxyenthalpic equivalents, and Hand, 1999, for interconversion of direct and indirect calorimetry for larvae of C. gigas and other species of mollusc). The energy consumed to synthesize the total amount of protein (536 ng) was calculated (1126 µJ) using a value of 2.1±0.2 kJ g −1 protein for larvae of C. gigas (Lee et al, 2016). Importantly, for this calculation of ATP allocation, the energy cost of protein synthesis is constantindependent of synthesis rate, genotype, growth phenotype and different environmental treatments of food, temperature and seawater pH (Lee et al, 2016;Pan et al, 2015a).…”

“…The energy consumed to synthesize the total amount of protein (536 ng) was calculated (1126 µJ) using a value of 2.1±0.2 kJ g −1 protein for larvae of C. gigas (Lee et al, 2016). Importantly, for this calculation of ATP allocation, the energy cost of protein synthesis is constantindependent of synthesis rate, genotype, growth phenotype and different environmental treatments of food, temperature and seawater pH (Lee et al, 2016;Pan et al, 2015a). The proportion of the ATP pool ( Fig.…”

“…During later growth of larval stages, fractional synthesis rates can exceed 100% (Carter and Houlihan, 2001). At such high rates of protein synthesis during development and growth, the energy cost of protein synthesis alone can account for the utilization of more than 50% of the total ATP pool (Lee et al, 2016;. Additionally, regulation of protein synthesis is a major biochemical response to alter metabolic status in response to environmental perturbation (Pan et al, 2015a;Hand, 2000, 2015).…”