Biochemical and metabolic effects on hydrogen isotope composition of organic compounds in plants

Abstract

Despite a large unexplained variability in the values, the analysis of the hydrogen (H) isotope composition (δ2H) of plant organic compounds is confidently applied to assess ecohydrological processes in the environment. This is possible because most studies that use the stable H isotopes from plant-derived biomarkers consider the H isotope fractionation that occurs during the biosynthesis of any given compound (2H-εbio) to be constant within a species. Consequently, 2H values in plant organic compounds are assumed to be mainly driven by the plant’s source water 2H values and the leaf water evaporative 2H-enrichment. There are, however, several indications that 2H-εbio of plant organic compounds can vary and that the δ2H values are also related to the plant’s metabolism. In this thesis, the elucidate the puzzling variability in the δ2H values of plant organic compounds, the influence of the plant’s metabolism on the variability of 2H-εbio is specifically explored with regards to the possible biochemical mechanisms underlying this variability. In a first study, based on empirical data produced in two separate experiments, it is shown that the 2H-εbio of different compounds in plants is tightly coupled to a plant’s carbon and energy metabolism. Based on these data, we develop a conceptual biochemical model that explains how and where 2H-fractionation occurs in the biosynthesis of major plant organic compound classes such as carbohydrates and lipids and what the isotope fractionation processes are that introduce a metabolic signal in δ2H values to these compounds. In a second study, with δ2H analyses from heterotrophic plants, it is shown that the hydrogen isotope fractionation occurring during the biosynthesis of different organic compounds in plants can explain part of the variability observed in δ2H values across species. Metabolic effects on 2H values between heterotrophic plants and their autotrophic host plants differed for different compound classes. The remarkable consistency of the compound specific isotope effects between autotrophic host or reference plants and the heterotrophic parasitic or mycoheterotrophic plants points towards a general physiological mechanism that determines these effects and support the model developed in the first study. Finally, with this model, it is mechanistically illustrated that information recorded in the δ2H values of plant organic compounds goes beyond hydrological signals, but also contains important information on the carbon and energy metabolism of a plant. As such we provide the mechanistic basis to introduce hydrogen isotopes in plant organic compounds as new metabolic proxy for the carbon and energy metabolism of plants. Such a new metabolic proxy has the potential to be applied in a broad range of disciplines, including plant and ecosystem physiology, plant breeding, biogeochemistry, paleoecology and Earth system sciences.