Abstract
Current knowledge of the mechanisms driving soil organic matter (SOM) turnover and responses to warming is mainly limited to surface soils, although over 50% of global soil carbon is contained in subsoils. Deep soils have different physicochemical properties, nutrient inputs, and microbiomes, which may harbor distinct functional traits and lead to different SOM dynamics and temperature responses. We hypothesized that kinetic and thermal properties of soil exoenzymes, which mediate SOM depolymerization, vary with soil depth, reflecting microbial adaptation to distinct substrate and temperature regimes. We determined the Michaelis-Menten (MM) kinetics of three ubiquitous enzymes involved in carbon (C), nitrogen (N) and phosphorus (P) acquisition at six soil depths down to 90 cm at a temperate forest, and their temperature sensitivity based on Arrhenius/Q10 and Macromolecular Rate Theory (MMRT) models over six temperatures between 4–50°C. Maximal enzyme velocity (Vmax) decreased strongly with depth for all enzymes, both on a dry soil mass and a microbial biomass C basis, whereas their affinities increased, indicating adaptation to lower substrate availability. Surprisingly, microbial biomass-specific catalytic efficiencies also decreased with depth, except for the P-acquiring enzyme, indicating distinct nutrient demands at depth relative to microbial abundance. These results suggested that deep soil microbiomes encode enzymes with intrinsically lower turnover and/or produce less enzymes per cell, reflecting distinct life strategies. The relative kinetics between different enzymes also varied with depth, suggesting an increase in relative P demand with depth, or that phosphatases may be involved in C acquisition. Vmax and catalytic efficiency increased consistently with temperature for all enzymes, leading to overall higher SOM-decomposition potential, but enzyme temperature sensitivity was similar at all depths and between enzymes, based on both Arrhenius/Q10 and MMRT models. In a few cases, however, temperature affected differently the kinetic properties of distinct enzymes at discrete depths, suggesting that it may alter the relative depolymerization of different compounds. We show that soil exoenzyme kinetics may reflect intrinsic traits of microbiomes adapted to distinct soil depths, although their temperature sensitivity is remarkably uniform. These results improve our understanding of critical mechanisms underlying SOM dynamics and responses to changing temperatures through the soil profile.
Highlights
Soils are estimated to contain ∼3,000 Gt carbon (C), which is more than all C in the atmosphere and in living biomass combined (Köchy et al, 2015)
We determined the MM kinetics of the enzymes acid phosphatase (AP), β-glucosidase (BG), and leucine aminopeptidase (LAP) in soils collected at six depth intervals from triplicate soil cores down to 90 cm (0–10, 10–20, 30–40, 50–60, 60–70, and 80– 90 cm), at six temperatures between 4 and 50◦C (4, 10, 16, 25, 35, or 50◦C) (Table 1)
We show that the temperature sensitivity of each enzyme is similar through the soil profile, based on both linear Arrhenius and non-linear Macromolecular Rate Theory (MMRT) models, temperature can directly affect the relative kinetics between enzyme types at discrete depths
Summary
Soils are estimated to contain ∼3,000 Gt carbon (C), which is more than all C in the atmosphere and in living biomass combined (Köchy et al, 2015). While current model predictions of C dynamics and responses to climate change are largely based on surface soils (Trumbore, 2009; Crowther et al, 2016; Van Gestel et al, 2018), soils below 20 cm contain up to 50% of the global soil C budget within the top 1 m of soil (Jobbágy and Jackson, 2000; Balesdent et al, 2018) These subsoils are predicted to warm at rates similar to those of surface soils (Soong et al, 2020), and recent in situ deep soil warming experiments have shown uniform warming responses down to 100–120 cm depth leading to soil C losses at least three times higher than those estimated based on surface soils alone (Hicks Pries et al, 2017; Hanson et al, 2020; Nottingham et al, 2020; Soong et al, 2021). Relatively little is known about the microbial mechanisms and interactions mediating SOM turnover and CO2 emissions, and their responses to environmental changes in subsoils (Rumpel and KögelKnabner, 2011; Gross and Harrison, 2019), which are essential to improve predictions of SOM dynamics in response to warming
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