Plant-soil synchrony in nutrient cycles: Learning from ecosystems to design sustainable agrosystems.

Redesigning agrosystems to include more ecological regulations can help feed a growing human population, preserve soils for future productivity, limit dependency on synthetic fertilizers, and reduce agriculture contribution to global changes such as eutrophication and warming. However, guidelines for redesigning cropping systems from natural systems to make them more sustainable remain limited. Synthetizing the knowledge on biogeochemical cycles in natural ecosystems, we outline four ecological systems that synchronize the supply of soluble nutrients by soil biota with the fluctuating nutrient demand of plants. This synchrony limits deficiencies and excesses of soluble nutrients, which usually penalize both production and regulating services of agrosystems such as nutrient retention and soil carbon storage. In the ecological systems outlined, synchrony emerges from plant-soil and plant-plant interactions, eco-physiological processes, soil physicochemical processes, and the dynamics of various nutrient reservoirs, including soil organic matter, soil minerals, atmosphere, and a common market. We discuss the relative importance of these ecological systems in regulating nutrient cycles depending on the pedoclimatic context and on the functional diversity of plants and microbes. We offer ideas about how these systems could be stimulated within agrosystems to improve their sustainability. A review of the latest advances in agronomy shows that some of the practices suggested to promote synchrony (e.g., reduced tillage, rotation with perennial plant cover, crop diversification) have already been tested and shown to be effective in reducing nutrient losses, fertilizer use, and N2 O emissions and/or improving biomass production and soil carbon storage. Our framework also highlights new management strategies and defines the conditions for the success of these nature-based practices allowing for site-specific modifications. This new synthetized knowledge should help practitioners to improve the long-term productivity of agrosystems while reducing the negative impact of agriculture on the environment and the climate.

Bioenergetic control of soil carbon dynamics across depth.

Soil carbon dynamics is strongly controlled by depth globally, with increasingly slow dynamics found at depth. The mechanistic basis remains however controversial, limiting our ability to predict carbon cycle-climate feedbacks. Here we combine radiocarbon and thermal analyses with long-term incubations in absence/presence of continuously 13C/14C-labelled plants to show that bioenergetic constraints of decomposers consistently drive the depth-dependency of soil carbon dynamics over a range of mineral reactivity contexts. The slow dynamics of subsoil carbon is tightly related to both its low energy density and high activation energy of decomposition, leading to an unfavourable 'return-on-energy-investment' for decomposers. We also observe strong acceleration of millennia-old subsoil carbon decomposition induced by roots ('rhizosphere priming'), showing that sufficient supply of energy by roots is able to alleviate the strong energy limitation of decomposition. These findings demonstrate that subsoil carbon persistence results from its poor energy quality together with the lack of energy supply by roots due to their low density at depth.

Catalytic power of enzymes decreases with temperature: New insights for understanding soil C cycling and microbial ecology under warming.

Most current models of soil C dynamics predict that climate warming will accelerate soil C mineralization, resulting in a long-term CO2 release and positive feedback to global warming. However, ecosystem warming experiments show that CO2 loss from warmed soils declines to control levels within a few years. Here, we explore the temperature dependence of enzymatic conversion of polymerized soil organic C (SOC) into assimilable compounds, which is presumed the rate-limiting step of SOC mineralization. Combining literature review, modelling and enzyme assays, we studied the effect of temperature on activity of enzymes considering their thermal inactivation and catalytic activity. We defined the catalytic power of enzymes (Epower ) as the cumulative amount of degraded substrate by one unit of enzyme until its complete inactivation. We show a universal pattern of enzyme's thermodynamic properties: activation energy of catalytic activity (EAcat ) < activation energy of thermal inactivation (EAinact ). By investing in stable enzymes (high EAinact ) having high catalytic activity (low EAcat ), microorganisms may maximize the Epower of their enzymes. The counterpart of such EAs' hierarchical pattern is the higher relative temperature sensitivity of enzyme inactivation than catalysis, resulting in a reduction in Epower under warming. Our findings could explain the decrease with temperature in soil enzyme pools, microbial biomass (MB) and carbon use efficiency (CUE) reported in some warming experiments and studies monitoring the seasonal variation in soil enzymes. They also suggest that a decrease in soil enzyme pools due to their faster inactivation under warming contributes to the observed attenuation of warming effect on soil C mineralization. This testable theory predicts that the ultimate response of SOC degradation to warming can be positive or negative depending on the relative temperature response of Epower and microbial production of enzymes.

Priming effect and microbial diversity in ecosystem functioning and response to global change: a modeling approach using the SYMPHONY model.

Integration of the priming effect (PE) in ecosystem models is crucial to better predict the consequences of global change on ecosystem carbon (C) dynamics and its feedbacks on climate. Over the last decade, many attempts have been made to model PE in soil. However, PE has not yet been incorporated into any ecosystem models. Here, we build plant/soil models to explore how PE and microbial diversity influence soil/plant interactions and ecosystem C and nitrogen (N) dynamics in response to global change (elevated CO2 and atmospheric N depositions). Our results show that plant persistence, soil organic matter (SOM) accumulation, and low N leaching in undisturbed ecosystems relies on a fine adjustment of microbial N mineralization to plant N uptake. This adjustment can be modeled in the SYMPHONY model by considering the destruction of SOM through PE, and the interactions between two microbial functional groups: SOM decomposers and SOM builders. After estimation of parameters, SYMPHONY provided realistic predictions on forage production, soil C storage and N leaching for a permanent grassland. Consistent with recent observations, SYMPHONY predicted a CO2 -induced modification of soil microbial communities leading to an intensification of SOM mineralization and a decrease in the soil C stock. SYMPHONY also indicated that atmospheric N deposition may promote SOM accumulation via changes in the structure and metabolic activities of microbial communities. Collectively, these results suggest that the PE and functional role of microbial diversity may be incorporated in ecosystem models with a few additional parameters, improving accuracy of predictions.