The metabolic basis of whole-organism RNA and phosphorus content

Abstract

Understanding the storage, flux, and turnover of nutrients in organisms is important for quantifying contributions of biota to biogeochemical cycles. Here we present a model that predicts the storage of phosphorus-rich RNA and whole-body phosphorus content in eukaryotes based on the mass- and temperature-dependence of ATP production in mitochondria. Data from a broad assortment of eukaryotes support the model's two main predictions. First, whole-body RNA concentration is proportional to mitochondrial density and consequently scales with body mass to the -1/4 power. Second, whole-body phosphorus content declines with increasing body mass in eukaryotic unicells but approaches a relatively constant value in large multicellular animals because the fraction of phosphorus in RNA decreases relative to the fraction in other pools. Extension of the model shows that differences in the flux of RNA-associated phosphorus are due to the size dependencies of metabolic rate and RNA concentration. Thus, the model explicitly links two biological currencies at the individual level: energy in the form of ATP and materials in the form of phosphorus, both of which are critical to the functioning of ecosystems. The model provides a framework for linking attributes of individuals to the storage and flux of phosphorus in ecosystems.

Fig. 1.

A log-log plot of whole-body RNA content corrected for the taxonspecific metabolic normalization constant, [RNA](b^′_o/b_o), as a function of dry body mass for unicellular eukaryotes, multicellular ectotherms, and endotherms. The solid line, fitted by using ordinary least-squares regression (y = -0.23x + 0.54), is close to the predicted dashed line of y =-0.25x + 0.61. Data and sources are listed in Table 2. The yeast species were standardized by using the estimated value of b_o for unicells.

Fig. 2.

The contribution of RNA to whole-body P content. (A) Effects of body size on P content only in RNA, [P_RNA], and in the whole body (RNA plus other pools) [P_body]. The dashed [P_RNA] line is predicted based on the relationship of [RNA] to body mass derived in Eq. 5 and shown in Fig. 1 ([P_RNA] = 0.037M^-0.25). The [P_body] line is predicted from Eq. 6 ([P_body] = [P_RNA] + [P_other]), with an estimate of [P_other] for invertebrates of 0.6% (12). Data shown are for adults of 169 insect species from the Sonoran desert (41). (B) The percentage of whole-body P contained in RNA for invertebrates and vertebrates as a function of body mass, i.e., 100 × [P_RNA]/([P_body]). The dashed line for invertebrates and the solid line for vertebrates are predicted from Eq. 6. For invertebrates, the parameter estimates used here are the same as those in A. For vertebrates, [P_other] is taken to be 2.4% (40), and the size dependence for [P_RNA] is taken to be [P_RNA] = 0.15M^-0.25 based on Eq. 5 and differences in b_o between endotherms and multicellular ectotherms. Data values and sources are listed in Table 2. Note that in A and B, the data cluster around the predicted lines and, thus, strongly support the model's predictions.