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Impact of climate warming on soil exoenzyme kinetic properties and their role in forecasting carbon flux

Periodic Reporting for period 1 - EUsoil-C-FLUX (Impact of climate warming on soil exoenzyme kinetic properties and their role in forecasting carbon flux)

Reporting period: 2020-09-01 to 2022-08-31

The majority of the Earth’s terrestrial carbon (C) is stored in the soil as organic carbon, at quantities more than three times the size of the atmospheric carbon pool. Response of this vast reservoir of C to climate change is highly uncertain, and changes may alter multiple soil ecosystem services such as climate regulation, food production and water purification. The overall objective of this Marie Skłodowska Curie Action (MSCA) - EUsoil-C-FLUX has been to understand how soil microorganisms and the exoenzyme they produce respond to climate warming. Tackling the challenge of evaluating the contribution of exoenzymes kinetic properties to soil respiration (Rsoil) and their potential adaptation to warming temperature is an utmost priority if we intend to better predict future shifts in the C cycle. The latter is a prerequisite to fulfilling a key priority of the European Union in reducing greenhouse gas emissions.
>The main objectives of this project have been to (i) determine and better understand the thermal adaptation of soil exoenzyme kinetic to their respective climate along altitudinal gradients in the Alps; (ii) to evaluate the ability of soil microbial community to acclimate to warmer climate condition by setting up a controlled warming experiment in a unique world-leading research facility (the European Ecotron of Montpellier); (iii) use cutting edge and interdisciplinary technologies (isotope labelling, high throughput DNA sequencing) to provide a detailed mechanistic understanding of soil respiration and microbial metabolism responses to warming. In parallel, (IV) the goal of this EUsoil-C-FLUX MSCA Individual Fellowship has been to enhance the Fellow (JP) career prospects through the training received on soil flux measurements, his supervisory role (master student) and his project leader role.
The research of the project was done in two main parts. We first (i) determined the local adaptation of soil exoenzyme kinetic properties (Vmax, Km) and the causal biotic mechanisms across altitudinal gradients in the Alps (WP1 - survey). To do so, 160 soil samples previously collected between 2016 and 2020 from the long-term observatory ORCHAMP were gathered by JP along with the associated metadata (climate data, soil properties). Working on soil samples from the ORCHAMPS observatory allowed us to sample soils from many climates. Soils were sampled from 24 altitudinal gradients along the French Alps, ranging from 300m a.s.l to more than 3100 m a.s.l. The mean annual temperature of those soils ranged from -3.5 to 12.5°C, and soil pH ranged from 3.5 to 7.8 providing thus an extensive range of abiotic conditions to better test our first hypothesis. Hydrolytic soil exoenzyme activities of phosphatase, β-glucosidase, acetyl esterase and leucine-aminopeptidase have been measured at eight temperatures ranging from 1°C to 45 °C in Montpellier. We applied the Arrhenius laws and the recently proposed macromolecular rate theory (MMRT) to describe the temperature response of exoenzymes. We also measured the thermal stability of soil exoenzymes by conditioning soil samples at 60°C for 24h. Interestingly, our research suggests the presence of an evolutionary trade-off between enzyme thermal stability and enzymes thermal sensitivity. Using linear mixed model averaging, we found that maximum annual temperature strongly influenced the sensitivity of enzymes involved in C acquisition (β-glucosidase) but not the other enzymes involved in N and P. This may indicate that temperature is the limiting factor for C-acquiring enzymes in alpine ecosystems with a potentially strong impact under a warming climate. This is particularly true concerning the large amount of old SOC stored in cold areas such as mountain soils, potentially highly vulnerable to climate change. Results from this first research part have been put together in a publication (in review) and were also presented at two international conferences. Two students that JP supervised participated in this first research part (a master's student and one graduate student (in 2021).
In the second research part of this project, the main objective was to test the hypothesis of exoenzyme thermal adaptation under controlled environment conditions (Ecotron) while evaluating for potential changes in soil microbial community structure, microbial biomass, and carbon use efficiency. To enhance the generality of findings, we selected ecosystems that maximise differences between samples in terms of climate (warm vs cold-adapted) and soil pH. Three altitudinal gradients, which ranged from acidic to alkaline bedrocks, were selected. For each gradient, the lowest and highest elevation sites were chosen to sample cold versus warm-adapted soil microbial communities. Soils from the targeted sites were sampled during the summer of 2021 and were subjected to warming treatments at the microcosm platform at the Ecotron in Montpellier. Surprisingly we did not find any acclimation of soil enzymes thermal sensitivity to 100 days of warming. This was also the case for the CUE thermal sensitivity assayed using the isotope water labelling (18O) method. This was a significant result of the project, as it is currently expected that soil microorganisms will adapt quickly to climate warming. This could have substantial implications as non-adapted microorganisms could increase soil organic carbon losses from the soil as CO2. To confirm these results, we seized the opportunity to sample alpine soils from an undergoing long-term climate warming experiment. We showed that the thermal sensitivity did not change after 5 years of warming treatment, and this was associated with a loss in soil organic carbon content of 15%.
The expected final result of the project is to provide an overarching study of the temperature response of soil enzymes to warming and its consequences on soil carbon flux. To my knowledge, this is the first time a study has provided a large-scale estimation of the temperature sensitivity of soil exoenzymes. Our results shed light on the variability of microbial enzyme decomposition thermal sensitivity between different ecosystems and what abiotic and biotic factors drive it. The temperature sensitivity of microbial decomposition is one of the main uncertainties of the carbon cycle model. Our results will benefit the community and modellers. Integration of new findings and data into mechanistic modelling will enhance predictions of the response of soil respiration (CO²) to warming in many habitats. This is ongoing work that JP will continue after the end of this MSCA project as a permanent researcher at CNRS. Data from this project are also included in an ongoing global collaborative article investigating the drivers of soil exoenzymes activity worldwide. As explained above, we did not find a quick acclimation of the thermal sensitivity of microbial enzymes and carbon use efficiency in response to warming. This surprising result paved the way for new research about the potential of acclimation of soil microbial community to climate disturbances and the consequences for ecosystem functioning. Finally, the differences observed in thermal sensitivity between alkaline and acidic soil environments may have importance for natural protection policy. Results from our MSCA project demonstrate that certain soils may be more sensitive to warming than others.
EUsoil-C-Flux project
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