Different “metabolomic niches” of the highly diverse tree species of the French Guiana rainforests

Abstract

Tropical rainforests harbor a particularly high plant diversity. We hypothesize that potential causes underlying this high diversity should be linked to distinct overall functionality (defense and growth allocation, anti-stress mechanisms, reproduction) among the different sympatric taxa. In this study we tested the hypothesis of the existence of a metabolomic niche related to a species-specific differential use and allocation of metabolites. We tested this hypothesis by comparing leaf metabolomic profiles of 54 species in two rainforests of French Guiana. Species identity explained most of the variation in the metabolome, with a species-specific metabolomic profile across dry and wet seasons. In addition to this "homeostatic" species-specific metabolomic profile significantly linked to phylogenetic distances, also part of the variance (flexibility) of the metabolomic profile was explained by season within a single species. Our results support the hypothesis of the high diversity in tropical forest being related to a species-specific metabolomic niche and highlight ecometabolomics as a tool to identify this species functional diversity related and consistent with the ecological niche theory.

Highly Species-Specific Foliar Metabolomes of Diverse Woody Species and Relationships with the Leaf Economics Spectrum

“…The huge diversity of specialized metabolites results from various metabolic pathways, in which variable combinations of precursor subunits are used, as well as from multi-member gene and enzyme families, multi-product enzymes, low substrate specificities of certain enzymes and various modifications of backbones (e.g., methylation, glycosylation) within substance classes [ 4 , 33 , 34 ]. Across plant species, the metabolite richness differs pronouncedly, as shown in the present study and in other studies for herbs and trees [ 9 , 13 , 35 ]. We cannot rule out that the variability in the metabolite numbers is partly related to different leaf matrices affecting metabolite extraction and detection.…”

“…When comparing the chemical composition among species, their phylogenetic relatedness should be taken into account, similarly as is done in comprehensive biodiversity studies [ 11 , 12 ]. Phylogenetic imprints in the metabolome are a result of past and current environmental factors that shape the metabolic composition of plants [ 4 ], leading to species-specific metabolomic niches [ 13 ]. Ecometabolomics tools are increasingly used to explore such taxon-related differences but also to uncover species-specific responses to certain environmental conditions [ 9 , 14 , 15 , 16 ].…”

“…Leaf habits are hence closely related to the leaf economics spectrum, with deciduousness being associated with acquisitive leaves and evergreenness with conservative ones. These different leaf strategies should be mirrored in foliar metabolism, as metabolic pathways are closely linked to leaf growth [ 20 ], photosynthesis [ 21 ] and allocation of resources [ 13 , 22 ]. Thus, distinct metabolomes for species of different functional types (i.e., deciduous versus evergreen) as well as links between the primary and specialized metabolome and leaf SLA, C and N can be expected.…”

Plot diversity differentially affects the chemical composition of leaves, roots and root exudates in four subtropical tree species

“…For example, total phenolic concentrations in birch ( Betula pendula ) leaves increased with plot diversity level (Poeydebat et al, 2020). So far, untargeted metabolomic approaches have been mostly used to quantify chemical diversity related to phylogenetic distances in large tropical tree genera (Endara et al, 2015, Salazar et al, 2018, Sedio, 2017), chemical diversity within canopies (Sedio et al, 2019, Sedio et al, 2017, Wiggins et al, 2016), induced responses, or variation in leaf metabolomes among seasons (Gargallo-Garriga et al, 2020). To our knowledge, none of these studies considered the effect of tree diversity levels as a driver of variation in tree metabolomes.…”

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

“…Previous studies have identified associations between species assemblages and habitat conditions in tropical rainforests [50][51][52][53], such as variations in leaf properties (parental material, drainage), leaf nutrient availability [14] and topography (slope steepness and orientation, margins with water courses), that are consistent with niche theory. Extensions of the classical ecological niche hypothesis, such as the biogeochemical niche hypothesis, claim that species tend to reach an optimal chemical composition that is linked to a singular optimal function (homeostasis) and allows niche occupation [54][55][56][57][58]. Thus, this study provides evidence for the use of a fundamental resource, such as the P, in the characterization of species niche space.…”