Different profiles of soil phosphorous compounds depending on tree species and availability of soil phosphorus in a tropical rainforest in French Guiana.

BACKGROUND: The availability of soil phosphorus (P) often limits the productivities of wet tropical lowland forests. Little is known, however, about the metabolomic profile of different chemical P compounds with potentially different uses and about the cycling of P and their variability across space under different tree species in highly diverse tropical rainforests. RESULTS: We hypothesised that the different strategies of the competing tree species to retranslocate, mineralise, mobilise, and take up P from the soil would promote distinct soil 31P profiles. We tested this hypothesis by performing a metabolomic analysis of the soils in two rainforests in French Guiana using 31P nuclear magnetic resonance (NMR). We analysed 31P NMR chemical shifts in soil solutions of model P compounds, including inorganic phosphates, orthophosphate mono- and diesters, phosphonates, and organic polyphosphates. The identity of the tree species (growing above the soil samples) explained > 53% of the total variance of the 31P NMR metabolomic profiles of the soils, suggesting species-specific ecological niches and/or species-specific interactions with the soil microbiome and soil trophic web structure and functionality determining the use and production of P compounds. Differences at regional and topographic levels also explained some part of the the total variance of the 31P NMR profiles, although less than the influence of the tree species. Multivariate analyses of soil 31P NMR metabolomics data indicated higher soil concentrations of P biomolecules involved in the active use of P (nucleic acids and molecules involved with energy and anabolism) in soils with lower concentrations of total soil P and higher concentrations of P-storing biomolecules in soils with higher concentrations of total P. CONCLUSIONS: The results strongly suggest "niches" of soil P profiles associated with physical gradients, mostly topographic position, and with the specific distribution of species along this gradient, which is associated with species-specific strategies of soil P mineralisation, mobilisation, use, and uptake.

Implications of mistletoe parasitism for the host metabolome: A new plant identity in the forest canopy.

Mistletoe-host systems exemplify an intimate and chronic relationship where mistletoes represent protracted stress for hosts, causing long-lasting impact. Although host changes in morphological and reproductive traits due to parasitism are well known, shifts in their physiological system, altering metabolite concentrations, are less known due to the difficulty of quantification. Here, we use ecometabolomic techniques in the plant-plant interaction, comparing the complete metabolome of the leaves from mistletoe (Viscum album) and needles from their host (Pinus nigra), both parasitized and unparasitized, to elucidate host responses to plant parasitism. Our results show that mistletoe acquires metabolites basically from the primary metabolism of its host and synthesizes its own defence compounds. In response to mistletoe parasitism, pines modify a quarter of their metabolome over the year, making the pine canopy metabolome more homogeneous by reducing the seasonal shifts in top-down stratification. Overall, host pines increase antioxidant metabolites, suggesting oxidative stress, and also increase part of the metabolites required by mistletoe, which act as a permanent sink of host resources. In conclusion, by exerting biotic stress and thereby causing permanent systemic change, mistletoe parasitism generates a new host-plant metabolic identity available in forest canopy, which could have notable ecological consequences in the forest ecosystem.

31P-NMR Metabolomics Revealed Species-Specific Use of Phosphorous in Trees of a French Guiana Rainforest.

Productivity of tropical lowland moist forests is often limited by availability and functional allocation of phosphorus (P) that drives competition among tree species and becomes a key factor in determining forestall community diversity. We used non-target 31P-NMR metabolic profiling to study the foliar P-metabolism of trees of a French Guiana rainforest. The objective was to test the hypotheses that P-use is species-specific, and that species diversity relates to species P-use and concentrations of P-containing compounds, including inorganic phosphates, orthophosphate monoesters and diesters, phosphonates and organic polyphosphates. We found that tree species explained the 59% of variance in 31P-NMR metabolite profiling of leaves. A principal component analysis showed that tree species were separated along PC 1 and PC 2 of detected P-containing compounds, which represented a continuum going from high concentrations of metabolites related to non-active P and P-storage, low total P concentrations and high N:P ratios, to high concentrations of P-containing metabolites related to energy and anabolic metabolism, high total P concentrations and low N:P ratios. These results highlight the species-specific use of P and the existence of species-specific P-use niches that are driven by the distinct species-specific position in a continuum in the P-allocation from P-storage compounds to P-containing molecules related to energy and anabolic metabolism.

Nutrient scarcity strengthens soil fauna control over leaf litter decomposition in tropical rainforests.

Soil fauna is a key control of the decomposition rate of leaf litter, yet its interactions with litter quality and the soil environment remain elusive. We conducted a litter decomposition experiment across different topographic levels within the landscape replicated in two rainforest sites providing natural gradients in soil fertility to test the hypothesis that low nutrient availability in litter and soil increases the strength of fauna control over litter decomposition. We crossed these data with a large dataset of 44 variables characterizing the biotic and abiotic microenvironment of each sampling point and found that microbe-driven carbon (C) and nitrogen (N) losses from leaf litter were 10.1 and 17.9% lower, respectively, in the nutrient-poorest site, but this among-site difference was equalized when meso- and macrofauna had access to the litterbags. Further, on average, soil fauna enhanced the rate of litter decomposition by 22.6%, and this contribution consistently increased as nutrient availability in the microenvironment declined. Our results indicate that nutrient scarcity increases the importance of soil fauna on C and N cycling in tropical rainforests. Further, soil fauna is able to equalize differences in microbial decomposition potential, thus buffering to a remarkable extent nutrient shortages at an ecosystem level.

Plant invasion is associated with higher plant-soil nutrient concentrations in nutrient-poor environments.

Plant invasion is an emerging driver of global change worldwide. We aimed to disentangle its impacts on plant-soil nutrient concentrations. We conducted a meta-analysis of 215 peer-reviewed articles and 1233 observations. Invasive plant species had globally higher N and P concentrations in photosynthetic tissues but not in foliar litter, in comparison with their native competitors. Invasive plants were also associated with higher soil C and N stocks and N, P, and K availabilities. The differences in N and P concentrations in photosynthetic tissues and in soil total C and N, soil N, P, and K availabilities between invasive and native species decreased when the environment was richer in nutrient resources. The results thus suggested higher nutrient resorption efficiencies in invasive than in native species in nutrient-poor environments. There were differences in soil total N concentrations but not in total P concentrations, indicating that the differences associated to invasive plants were related with biological processes, not with geochemical processes. The results suggest that invasiveness is not only a driver of changes in ecosystem species composition but that it is also associated with significant changes in plant-soil elemental composition and stoichiometry.

Shifts in plant foliar and floral metabolomes in response to the suppression of the associated microbiota.

BACKGROUND: The phyllospheric microbiota is assumed to play a key role in the metabolism of host plants. Its role in determining the epiphytic and internal plant metabolome, however, remains to be investigated. We analyzed the Liquid Chromatography-Mass Spectrometry (LC-MS) profiles of the epiphytic and internal metabolomes of the leaves and flowers of Sambucus nigra with and without external antibiotic treatment application. RESULTS: The epiphytic metabolism showed a degree of complexity similar to that of the plant organs. The suppression of microbial communities by topical applications of antibiotics had a greater impact on the epiphytic metabolome than on the internal metabolomes of the plant organs, although even the latter changed significantly both in leaves and flowers. The application of antibiotics decreased the concentration of lactate in both epiphytic and organ metabolomes, and the concentrations of citraconic acid, acetyl-CoA, isoleucine, and several secondary compounds such as terpenes and phenols in the epiphytic extracts. The metabolite pyrogallol appeared in the floral epiphytic community only after the treatment. The concentrations of the amino acid precursors of the ketoglutarate-synthesis pathway tended to decrease in the leaves and to increase in the foliar epiphytic extracts. CONCLUSIONS: These results suggest that anaerobic and/or facultative anaerobic bacteria were present in high numbers in the phyllosphere and in the apoplasts of S. nigra. The results also show that microbial communities play a significant role in the metabolomes of plant organs and could have more complex and frequent mutualistic, saprophytic, and/or parasitic relationships with internal plant metabolism than currently assumed.

Warming differentially influences the effects of drought on stoichiometry and metabolomics in shoots and roots.

Plants in natural environments are increasingly being subjected to a combination of abiotic stresses, such as drought and warming, in many regions. The effects of each stress and the combination of stresses on the functioning of shoots and roots have been studied extensively, but little is known about the simultaneous metabolome responses of the different organs of the plant to different stresses acting at once. We studied the shift in metabolism and elemental composition of shoots and roots of two perennial grasses, Holcus lanatus and Alopecurus pratensis, in response to simultaneous drought and warming. These species responded differently to individual and simultaneous stresses. These responses were even opposite in roots and shoots. In plants exposed to simultaneous drought and warming, terpenes, catechin and indole acetic acid accumulated in shoots, whereas amino acids, quinic acid, nitrogenous bases, the osmoprotectants choline and glycine betaine, and elements involved in growth (nitrogen, phosphorus and potassium) accumulated in roots. Under drought, warming further increased the allocation of primary metabolic activity to roots and changed the composition of secondary metabolites in shoots. These results highlight the plasticity of plant metabolomes and stoichiometry, and the different complementary responses of shoots and roots to complex environmental conditions.

Drought enhances folivory by shifting foliar metabolomes in Quercus ilex trees.

At the molecular level, folivory activity on plants has mainly been related to the foliar concentrations of nitrogen (N) and/or particular metabolites. We studied the responses of different nutrients and the whole metabolome of Quercus ilex to seasonal changes and to moderate field experimental conditions of drought, and how this drought may affect folivory activity, using stoichiometric and metabolomic techniques. Foliar potassium (K) concentrations increased in summer and consequently led to higher foliar K : phosphorus (P) and lower carbon (C) : K and N : K ratios. Foliar N : P ratios were not lowest in spring as expected by the growth rate hypothesis. Trees exposed to moderate drought presented higher concentrations of total sugars and phenolics and these trees also experienced more severe folivory attack. The foliar increases in K, sugars and antioxidant concentrations in summer, the driest Mediterranean season, indicated enhanced osmoprotection under natural drought conditions. Trees under moderate drought also presented higher concentrations of sugars and phenolics; a plant response to avoid water loss. These shifts in metabolism produced an indirect relationship between increased drought and folivory activity.

Foliar elementome and functional traits relationships identify tree species niche in French Guiana rainforests.

Biogeochemical niche (BN) hypothesis aims to relate species/genotype elemental composition with its niche based on the fact that different elements are involved differentially in distinct plant functions. We here test the BN hypothesis through the analysis of the 10 foliar elemental concentrations and 20 functional-morphological of 60 tree species in a French Guiana tropical forest. We observed strong legacy (phylogenic + species) signals in the species-specific foliar elemental composition (elementome) and, for the first time, provide empirical evidence for a relationship between species-specific foliar elementome and functional traits. Our study thus supports the BN hypothesis and confirms the general niche segregation process through which the species-specific use of bio-elements drives the high levels of α-diversity in this tropical forest. We show that the simple analysis of foliar elementomes may be used to test for BNs of co-occurring species in highly diverse ecosystems, such as tropical rainforests. Although cause and effect mechanisms of leaf functional and morphological traits in species-specific use of bio-elements require confirmation, we posit the hypothesis that divergences in functional-morphological niches and species-specific biogeochemical use are likely to have co-evolved.

Leaf metabolic traits reveal hidden dimensions of plant form and function.

The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization-a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

Contrasting nitrogen and phosphorus fertilization effects on soil terpene exchanges in a tropical forest.

Production, emission, and absorption of biogenic volatile organic compounds (BVOCs) in ecosystem soils and associated impacts of nutrient availability are unclear; thus, predictions of effects of global change on source-sink dynamic under increased atmospheric N deposition and nutrition imbalances are limited. Here, we report the dynamics of soil BVOCs under field conditions from two undisturbed tropical rainforests from French Guiana. We analyzed effects of experimental soil applications of nitrogen (N), phosphorus (P), and N + P on soil BVOC exchanges (in particular of total terpenes, monoterpenes, and sesquiterpenes), to determine source and sink dynamics between seasons (dry and wet) and elevations (upper and lower elevations corresponding to top of the hills (30 m high) and bottom of the valley). We identified 45 soil terpenoids compounds emitted to the atmosphere, comprising 26 monoterpenes and 19 sesquiterpenes; of these, it was possible to identify 13 and 7 compounds, respectively. Under ambient conditions, soils acted as sinks of these BVOCs, with greatest soil uptake recorded for sesquiterpenes at upper elevations during the wet season (-282 µg m-2 h-1). Fertilization shifted soils from a sink to source, with greatest levels of terpene emissions recorded at upper elevations during the wet season, following the addition of N (monoterpenes: 406 µg m-2 h-1) and P (sesquiterpenes: 210 µg m-2 h-1). Total soil terpene emission rates were negatively correlated with total atmospheric terpene concentrations. These results indicate likely shifts in tropical soils from sink to source of atmospheric terpenes under projected increases in N deposition under global change, with potential impacts on regional-scale atmospheric chemistry balance and ecosystem function.

Decay of similarity across tropical forest communities: integrating spatial distance with soil nutrients.

Understanding the mechanisms that drive the change of biotic assemblages over space and time is the main quest of community ecology. Assessing the relative importance of dispersal and environmental species selection in a range of organismic sizes and motilities has been a fruitful strategy. A consensus for whether spatial and environmental distances operate similarly across spatial scales and taxa, however, has yet to emerge. We used censuses of four major groups of organisms (soil bacteria, fungi, ground insects, and trees) at two observation scales (1-m2 sampling point vs. 2,500-m2 plots) in a topographically standardized sampling design replicated in two tropical rainforests with contrasting relationships between spatial distance and nutrient availability. We modeled the decay of assemblage similarity for each taxon set and site to assess the relative contributions of spatial distance and nutrient availability distance. Then, we evaluated the potentially structuring effect of tree composition over all other taxa. The similarity of nutrient content in the litter and topsoil had a stronger and more consistent selective effect than did dispersal limitation, particularly for bacteria, fungi, and trees at the plot level. Ground insects, the only group assessed with the capacity of active dispersal, had the highest species turnover and the flattest nonsignificant distance-decay relationship, suggesting that neither dispersal limitation nor nutrient availability were fundamental drivers of their community assembly at this scale of analysis. Only the fungal communities at one of our study sites were clearly coordinated with tree composition. The spatial distance at the smallest scale was more important than nutrient selection for the bacteria, fungi, and insects. The lower initial similarity and the moderate variation in composition identified by these distance-decay models, however, suggested that the effects of stochastic sampling were important at this smaller spatial scale. Our results highlight the importance of nutrients as one of the main environmental drivers of rainforest communities irrespective of organismic or propagule size and how the overriding effect of the analytical scale influences the interpretation, leading to the perception of greater importance of dispersal limitation and ecological drift over selection associated with environmental niches at decreasing observation scales.

Metabolome-Wide, Phylogenetically Controlled Comparison Indicates Higher Phenolic Diversity in Tropical Tree Species.

Tropical plants are expected to have a higher variety of defensive traits, such as a more diverse array of secondary metabolic compounds in response to greater pressures of antagonistic interactions, than their temperate counterparts. We test this hypothesis using advanced metabolomics linked to a novel stoichiometric compound classification to analyze the complete foliar metabolomes of four tropical and four temperate tree species, which were selected so that each subset contained the same amount of phylogenetic diversity and evenness. We then built Bayesian phylogenetic multilevel models to test for tropical-temperate differences in metabolite diversity for the entire metabolome and for four major families of secondary compounds. We found strong evidence supporting that the leaves of tropical tree species have a higher phenolic diversity. The functionally closer group of polyphenolics also showed moderate evidence of higher diversity in tropical species, but there were no differences either for the entire metabolome or for the other major families of compounds analyzed. This supports the interpretation that this tropical-temperate contrast must be related to the functional role of phenolics and polyphenolics.

Tree Species and Epiphyte Taxa Determine the "Metabolomic niche" of Canopy Suspended Soils in a Species-Rich Lowland Tropical Rainforest.

Tropical forests are biodiversity hotspots, but it is not well understood how this diversity is structured and maintained. One hypothesis rests on the generation of a range of metabolic niches, with varied composition, supporting a high species diversity. Characterizing soil metabolomes can reveal fine-scale differences in composition and potentially help explain variation across these habitats. In particular, little is known about canopy soils, which are unique habitats that are likely to be sources of additional biodiversity and biogeochemical cycling in tropical forests. We studied the effects of diverse tree species and epiphytes on soil metabolomic profiles of forest floor and canopy suspended soils in a French Guianese rainforest. We found that the metabolomic profiles of canopy suspended soils were distinct from those of forest floor soils, differing between epiphyte-associated and non-epiphyte suspended soils, and the metabolomic profiles of suspended soils varied with host tree species, regardless of association with epiphyte. Thus, tree species is a key driver of rainforest suspended soil metabolomics. We found greater abundance of metabolites in suspended soils, particularly in groups associated with plants, such as phenolic compounds, and with metabolic pathways related to amino acids, nucleotides, and energy metabolism, due to the greater relative proportion of tree and epiphyte organic material derived from litter and root exudates, indicating a strong legacy of parent biological material. Our study provides evidence for the role of tree and epiphyte species in canopy soil metabolomic composition and in maintaining the high levels of soil metabolome diversity in this tropical rainforest. It is likely that a wide array of canopy microsite-level environmental conditions, which reflect interactions between trees and epiphytes, increase the microscale diversity in suspended soil metabolomes.

Empirical support for the biogeochemical niche hypothesis in forest trees.

The possibility of using the elemental compositions of species as a tool to identify species/genotype niche remains to be tested at a global scale. We investigated relationships between the foliar elemental compositions (elementomes) of trees at a global scale with phylogeny, climate, N deposition and soil traits. We analysed foliar N, P, K, Ca, Mg and S concentrations in 23,962 trees of 227 species. Shared ancestry explained 60-94% of the total variance in foliar nutrient concentrations and ratios whereas current climate, atmospheric N deposition and soil type together explained 1-7%, consistent with the biogeochemical niche hypothesis which predicts that each species will have a specific need for and use of each bio-element. The remaining variance was explained by the avoidance of nutritional competition with other species and natural variability within species. The biogeochemical niche hypothesis is thus able to quantify species-specific tree niches and their shifts in response to environmental changes.

High foliar K and P resorption efficiencies in old-growth tropical forests growing on nutrient-poor soils.

Resorption is the active withdrawal of nutrients before leaf abscission. This mechanism represents an important strategy to maintain efficient nutrient cycling; however, resorption is poorly characterized in old-growth tropical forests growing in nutrient-poor soils. We investigated nutrient resorption from leaves in 39 tree species in two tropical forests on the Guiana Shield, French Guiana, to investigate whether resorption efficiencies varied with soil nutrient, seasonality, and species traits. The stocks of P in leaves, litter, and soil were low at both sites, indicating potential P limitation of the forests. Accordingly, mean resorption efficiencies were higher for P (35.9%) and potassium (K; 44.6%) than for nitrogen (N; 10.3%). K resorption was higher in the wet (70.2%) than in the dry (41.7%) season. P resorption increased slightly with decreasing total soil P; and N and P resorptions were positively related to their foliar concentrations. We conclude that nutrient resorption is a key plant nutrition strategy in these old-growth tropical forests, that trees with high foliar nutrient concentration reabsorb more nutrient, and that nutrients resorption in leaves, except P, are quite decoupled from nutrients in the soil. Seasonality and biochemical limitation played a role in the resorption of nutrients in leaves, but species-specific requirements obscured general tendencies at stand and ecosystem level.

Comparable canopy and soil free-living nitrogen fixation rates in a lowland tropical forest.

Biological nitrogen fixation (BNF) is a fundamental part of nitrogen cycling in tropical forests, yet little is known about the contribution made by free-living nitrogen fixers inhabiting the often-extensive forest canopy. We used the acetylene reduction assay, calibrated with 15N2, to measure free-living BNF on forest canopy leaves, vascular epiphytes, bryophytes and canopy soil, as well as on the forest floor in leaf litter and soil. We used a combination of calculated and published component densities to upscale free-living BNF rates to the forest level. We found that bryophytes and leaves situated in the canopy in particular displayed high mass-based rates of free-living BNF. Additionally, we calculated that nearly 2 kg of nitrogen enters the forest ecosystem through free-living BNF every year, 40% of which was fixed by the various canopy components. Our results reveal that in the studied tropical lowland forest a large part of the nitrogen input through free-living BNF stems from the canopy, but also that the total nitrogen inputs by free-living BNF are lower than previously thought and comparable to the inputs of reactive nitrogen by atmospheric deposition.

Could Global Intensification of Nitrogen Fertilisation Increase Immunogenic Proteins and Favour the Spread of Coeliac Pathology?

Fertilisation of cereal crops with nitrogen (N) has increased in the last five decades. In particular, the fertilisation of wheat crops increased by nearly one order of magnitude from 1961 to 2010, from 9.84 to 93.8 kg N ha-1 y-1. We hypothesized that this intensification of N fertilisation would increase the content of allergenic proteins in wheat which could likely be associated with the increased pathology of coeliac disease in human populations. An increase in the per capita intake of gliadin proteins, the group of gluten proteins principally responsible for the development of coeliac disease, would be the responsible factor. We conducted a global meta-analysis of available reports that supported our hypothesis: wheat plants growing in soils receiving higher doses of N fertilizer have higher total gluten, total gliadin, α/ß-gliadin, γ-gliadin and ω-gliadin contents and higher gliadin transcription in their grain. We thereafter calculated the per capita annual average intake of gliadins from wheat and derived foods and found that it increased from 1961 to 2010 from approximately 2.4 to 3.8 kg y-1 per capita (+1.4 ± 0.18 kg y-1 per capita, mean ± SE), i.e., increased by 58 ± 7.5%. Finally, we found that this increase was positively correlated with the increase in the rates of coeliac disease in all the available studies with temporal series of coeliac disease. The impacts and damage of over-fertilisation have been observed at an environmental scale (e.g., eutrophication and acid rain), but a potential direct effect of over-fertilisation is thus also possible on human health (coeliac disease).

Higher fluxes of C, N and P in plant/soil cycles associated with plant invasion in a subtropical estuarine wetland in China.

Invasion of plants in wetland ecosystems is often associated with changes in litter decomposition and in nutrient use, uptake and cycling between invasive and native plants. We studied litter decomposition rates, N and P release and elemental composition and stoichiometry during the invasion of Phragmites australis and Spartina alterniflora into native Cyperus malaccensis wetlands in the Minjiang River estuary (China). Aboveground litter in mono-specific stands decomposed faster for Cyperus malaccensis than for Spartina alterniflora and for Phragmites australis. Cyperus malaccensis litter decomposed slower under the stands of both invasive species. In contrast, the litter of both invasive species decomposed faster under Cyperus malaccesis stands. We observed that the invasion of these species was associated with an increased rate of aboveground litter decomposition and large absolute amounts of C, N and P released from the litter when litter from invasive species was mixed with that of native species. Our results suggest that the large nutrient release from litter during early stages of the invasion favored invasive species with larger size and higher nutrient-uptake capacity than the native species.

Ecometabolomics for a Better Understanding of Plant Responses and Acclimation to Abiotic Factors Linked to Global Change.

The number of ecometabolomic studies, which use metabolomic analyses to disentangle organisms' metabolic responses and acclimation to a changing environment, has grown exponentially in recent years. Here, we review the results and conclusions of ecometabolomic studies on the impacts of four main drivers of global change (increasing frequencies of drought episodes, heat stress, increasing atmospheric carbon dioxide (CO2) concentrations and increasing nitrogen (N) loads) on plant metabolism. Ecometabolomic studies of drought effects confirmed findings of previous target studies, in which most changes in metabolism are characterized by increased concentrations of soluble sugars and carbohydrate derivatives and frequently also by elevated concentrations of free amino acids. Secondary metabolites, especially flavonoids and terpenes, also commonly exhibited increased concentrations when drought intensified. Under heat and increasing N loads, soluble amino acids derived from glutamate and glutamine were the most responsive metabolites. Foliar metabolic responses to elevated atmospheric CO2 concentrations were dominated by greater production of monosaccharides and associated synthesis of secondary metabolites, such as terpenes, rather than secondary metabolites synthesized along longer sugar pathways involving N-rich precursor molecules, such as those formed from cyclic amino acids and along the shikimate pathway. We suggest that breeding for crop genotypes tolerant to drought and heat stress should be based on their capacity to increase the concentrations of C-rich compounds more than the concentrations of smaller N-rich molecules, such as amino acids. This could facilitate rapid and efficient stress response by reducing protein catabolism without compromising enzymatic capacity or increasing the requirement for re-transcription and de novo biosynthesis of proteins.