Revisiting the growth rate hypothesis: Towards a holistic stoichiometric understanding of growth

Abstract

The growth rate hypothesis (GRH) posits that variation in organismal stoichiometry (C:P and N:P ratios) is driven by growth-dependent allocation of P to ribosomal RNA. The GRH has found broad but not uniform support in studies across diverse biota and habitats. We synthesise information on how and why the tripartite growth-RNA-P relationship predicted by the GRH may be uncoupled and outline paths for both theoretical and empirical work needed to broaden the working domain of the GRH. We found strong support for growth to RNA (r² = 0.59) and RNA-P to P (r² = 0.63) relationships across taxa, but growth to P relationships were relatively weaker (r² = 0.09). Together, the GRH was supported in ~50% of studies. Mechanisms behind GRH uncoupling were diverse but could generally be attributed to physiological (P accumulation in non-RNA pools, inactive ribosomes, translation elongation rates and protein turnover rates), ecological (limitation by resources other than P), and evolutionary (adaptation to different nutrient supply regimes) causes. These factors should be accounted for in empirical tests of the GRH and formalised mathematically to facilitate a predictive understanding of growth.

Keywords: RNA; carbon; ecological stoichiometry; growth rate hypothesis; nitrogen; phosphorus; protein.

FIGURE 1

A schematic diagram of the growth rate hypothesis (GRH). Tripartite relationships that constitute the GRH (black arrows) are shown linking organismal %P, growth rate and RNA allocation, as well as potential ecological, evolutionary and genomic drivers and consequences of that coupling (grey). Note that a focus is placed on P content as it is most often the primary driver of variation in organismal C:P and N:P ratios (rather than variation in %C or %N).

FIGURE 2

(a) A schematic depiction of four mechanisms that can influence the coupling of growth, RNA and P proposed by the GRH. On the organismal scale, the first mechanism (M1) involves contributions from pools of non‐RNA P, including storage of P in molecules such as polyphosphates. Mechanisms M2, M3 and M4 constitute changes on the molecular scale that individually or collectively affect the net protein production rate per ribosome. Mechanism (M2) involves change of the fraction of inactive ribosomes among all ribosomes. Mechanism (M3) entails differences in ribosome translation elongation rate and mechanism (M4) highlights protein degradation or protein turnover rate. (b) Effects of C‐, N‐ and P‐limitation on cellular functions. The figure shows the relationships between environmental resource supplies and cellular functions that influence growth rate and could result in deviations from the GRH under different types of resource limitation.

FIGURE 3

A conceptual depiction of scenarios that support or deviate from the GRH. Each line depicts a relationship between organismal growth rate (μ) and %P or %RNA. In each panel, intra‐specific data (individual lines) represent physiological and ontogenic responses within a taxon while inter‐specific patterns (comparisons of different lines) depict evolutionary differences among taxa: (a) GRH supported intra‐ and inter‐specifically, (b) GRH supported intra‐specifically but not inter‐specifically, (c) GRH supported inter‐specifically but not intra‐specifically (note that this is the current assumption of many stoichiometric models), (d) GRH contradicted intra‐specifically but supported inter‐specifically, (e) GRH supported intra‐specifically but contradicted inter‐specifically, and (f) GRH contradicted both inter‐specifically and intra‐specifically.

FIGURE 4

Theoretical relationships between organismal RNA and P. Relationships between organismal dry mass contributed by P found in RNA (%RNA‐P) and total organismal P content (%P) of an organism are depicted using an individual line for each species, genotype or ontogenetic stage. (A) GRH supported where all P is in the RNA pool (not physiologically possible), (B) GRH supported and RNA accounts for all variation in body %P, (B′) GRH supported but an organism is reallocating part its internal P pool to RNA, (B″) GRH supported but an organism is increasing allocation to P in other pools in addition to RNA, (C) GRH supported but not important (i.e., growth‐driven change in P is trivial), (D) GRH not supported due to shifts of stored P to RNA, (D′) GRH not supported because an organism is reducing its growth rate (right to left) and accumulating excess P for diapause, and (D″) GRH not supported due to P storage.

FIGURE 5

Empirical relationships between organismal %RNA‐P and total body %P. Linear regressions (dark black lines with 95% confidence intervals) across species were significant both for individual studies (a) that confirmed the GRH and (b) those that did not confirm the GRH. Reaction norms for (c) individual studies with slopes ≅ to 1 (d) >1, (e) <1 and (f) non‐significant slopes (p > 0.05) are also shown. Solid reaction norm lines indicate individual experiments confirming the GRH, and dotted lines are non‐confirmatory experiments. Note that realistic %RNA‐P and %P relationships are only possible above the 1:1 line.

FIGURE 6

Relationships between organismal growth and body P content. Significant non‐linear relationships (p < 0.001; r ² = 0.09) were found between (a) growth rates and %P across taxa using a general additive model (GAM; white and black solid line with 95% confidence intervals shown in dashed lines). Growth and %P increased linearly up to a growth threshold of 0.89 d⁻¹ (dashed vertical line), identified from the first derivative of the GAM. The linear portion of the curve was also modelled separately using an ordinary linear regression in panel B (p < 0.001; r ² = 0.04; slope = 0.45). Positive growth‐P reaction norms for individual datasets are shown in panel C and a subset of responses for organisms growing <2.0 d⁻¹ are shown in panel D for clarity. Non‐significant (p > 0.05) responses are depicted in panel E, and significant negative relationships between growth and %P are shown in panel F.