Dramatic biases in terrestrial nitrogen fixation in Earth System Models revealed by natural isotope signatures

Biological nitrogen fixation (BNF) is the primary input of new reactive nitrogen to natural terrestrial ecosystems. However, this flux is poorly constrained due to its unclear drivers and associated control mechanisms. Here, we extend the existing theory of nitrogen (N) isotope mass balance to estimate BNF rates and then use a Bayesian approach to constrain the BNF rates in natural terrestrial ecosystems by using measurements of natural N-isotope ratios (δ¹⁵N) in plants (δ_P) and soil (δ_S). Together with pairwise δ_P and δ_S measurements from 18 forest sites covering diverse climates and thousands of δ_P and δ_S observations worldwide, we show that the spatial distribution of the fraction of symbiotic BNF relative to the total external N acquisition by plants (f _BNFs) is primarily controlled by temperature (29%) and mycorrhizal fungi (14%), with colder climate and higher ectomycorrhizal fungi abundance leading to a lower f _BNFs. We find a large discrepancy between the spatial distributions of isotope-based BNF and those simulated by using Earth System Models (ESMs) in the Sixth Phase of the Coupled Model Intercomparison Project (CMIP6). Moreover, we constrain the global total BNF from natural terrestrial ecosystems as 78.2-89.8 Tg N yr^-1, suggesting a ≥18% underestimation of the global BNF in CMIP6 models. In addition to the temperature dependence found in previous laboratory studies, our isotope-based study suggests a competitive relationship between BNF and mycorrhizal N uptake as another important control mechanism. This complex interplay remains unresolved in ESMs and has the potential to improve BNF simulations in the next phase of CMIP.