Biological stoichiometry from genes to ecosystems

Abstract

Ecological stoichiometry is the study of the balance of multiple chemical elements in ecological interactions. This paper reviews recent findings in this area and seeks to broaden the stoichiometric concept for use in evolutionary studies, in integrating ecological dynamics with cellular and genetic mechanisms, and in developing a unified means for studying diverse organisms in diverse habitats. This broader approach would then be considered``biological stoichiometry''. Evidence supporting a hypothesised connection between the C:N:P stoichiometry of an organism and its growth rate (the``growth rate hypothesis'') is reviewed. Various data indicate that rapidly growing organisms commonly have low biomass C:P and N:P ratios. Evidence is then discussed suggesting that low C:P and N:P ratios in rapidly growing organisms reflect increased allocation to P-rich ribosomal RNA (rRNA), as rapid protein synthesis by ribosomes is required to support fast growth. Indeed, diverse organisms (bacteria, copepods, fishes, others) exhibit increased RNA levels when growing actively. This implies that evolutionary processes that generate, directly or indirectly, variation in a major life history trait (specific growth rate) have consequences for ecological dynamics due to their effects on organismal elemental composition. Genetic mechanisms by which organisms generate high RNA, high growth rate phenotypes are discussed next, focusing on the structure and organisation of the ribosomal RNA genes (the``rDNA''). In particular, published studies of a variety of taxa suggest an association between growth rate and variation in the length and content of the intergenic spacer (IGS) region of the rDNA tandem repeat unit. In particular, under conditions favouring increased growth or yield, the number of repeat units (``enhancers'') increases (and the IGS increases in length), and transcription rates of rRNA increase. In addition, there is evidence in the literature that increased numbers of copies of rDNA genes are associated with increased growth and production. Thus, a combination of genetic mechanisms may be responsible for establishing the growth potential, and thus the RNA allocation and C:N:P composition, of an organism. Furthermore, various processes, during both sexual and asexual reproduction, can generate variation in the rDNA to provide the raw material for selection and to generate ecologically significant variation in C:N:P stoichiometry. This leads us to hypothesize that the continuous generation of such variation may also play a role in how species interactions develop in ecosystems under different conditions of energy input and nutrient supply.

C: N: P stoichiometry and specific growth rate of clover colonized by arbuscular mycorrhizal fungi

“…Ecological stoichiometry is the study of the mass balance of multiple chemical elements in living systems (Reiners 1986;Hessen and Lyche 1991;Sterner 1995;Elser et al 1996Elser et al , 2000a, and recent advances have raised new questions about the implications of ecological stoichiometry for nutrient cycling and the functioning of organisms and communities of organisms in aquatic as well as terrestrial ecosystems (Elser et al 1996;Elser and Urabe 1999;Daufresne and Loreau 2001;Sterner and Elser 2002;Vrede et al 2004). In particular, the dynamics of carbon (C), nitrogen (N) and phosphorus (P) have been considered to be important in this context because these elements are both structurally and functionally essential in all organisms (Sterner 1995;Elser et al 1996;Vrede et al 2004).…”

“…Recent studies have suggested a mechanistic linkage between tissue elemental stoichiometry and the growth rate of the organism (Elser et al 2000a; Kyle et al 2003). The Growth Rate Hypothesis (GRH) proposes that higher growth rates are coupled not only to lower C: N and C: P ratios, but also to lower N: P ratio, and the variation in P concentration in organisms is driven by differences in allocation to P-rich ribosomal RNA (rRNA) needed to meet the protein synthesis demands of increased growth rates (Hessen and Lyche 1991;Elser et al 1996Elser et al , 2000aVrede et al 2004;Hessen et al 2007).…”

“…The Growth Rate Hypothesis (GRH) proposes that higher growth rates are coupled not only to lower C: N and C: P ratios, but also to lower N: P ratio, and the variation in P concentration in organisms is driven by differences in allocation to P-rich ribosomal RNA (rRNA) needed to meet the protein synthesis demands of increased growth rates (Hessen and Lyche 1991;Elser et al 1996Elser et al , 2000aVrede et al 2004;Hessen et al 2007). This GRH potentially connects cellular allocation to organism function and ultimately to ecological dynamics.…”

Stoichiometric controls of mercury dilution by growth

“…High availability of P relative to N (i.e., low N:P) results in a low algal N:P ratio (indicative of high algal quality as food), causing rapid growth in zooplankton, particularly Daphnia (4,16). A large body of work has found that Daphnia consistently grow more efficiently on phytoplankton with high P content relative to N or C (16-18) because of their high P demand for protein synthesis (19). Hence, SGD may cause zooplankton in lakes with low N:P algae to have lower MeHg concentrations.…”

Antibiotic‐induced effects on scaling relationships and on plant element contents in herbs and grasses

“…Carbon (C), nitrogen (N), and phosphorus (P) are three of the most important elements for plants, and their concentration in plant biomass is directly related to the plant's performance. For example, fast‐growing species have a high biomass P:C ratio and a low biomass N:P ratio, due to higher production of P‐rich ribosomal RNA relative to N‐rich chloroplasts (Growth Rate Hypothesis, see Ågren, 2004; Elser et al., 2000; Sterner & Elser, 2002). In total, plants require about 30 different elements, some in large quantities (macroelements, e.g., H, C, N, O, P, S, K, Ca), others in small quantities (microelements, e.g., Mn, Zn, Fe, Mo) (Ågren, 2008).…”