Modelling in situ activities of enzymes as a tool to explain seasonal variation of soil respiration from agro-ecosystems
Introduction
Soil carbon (C) stock is estimated to be >1500 Pg C, significantly higher than atmospheric stock ∼750 Pg C (Kirschbaum, 2000, Davidson and Janssens, 2006, IPCC, 2007). SOC, the largest pool in terrestrial C cycling (Kandeler et al., 2005), has the potential to act as a source or sink of greenhouse gases due to its dynamic interactions with the atmosphere (Lal, 2004). A large fraction of C is introduced into the atmosphere as CO2 through microbial decomposition of organic matter (Frey et al., 2013). Temperature sensitivity of soil organic matter (SOM) decomposition has been given great attention (Davidson et al., 2012) due to the inherent relevance of kinetic theory (Davidson and Janssens, 2006). Expected warming of the earth's climate between 3 and 5 °C over the next century (Bergfur and Friberg, 2012) may accelerate decomposition of SOC (Bengtson and Bengtsson, 2007) through faster processing of SOC by soil biotic communities and, therefore, affect the C source or sink functions of soils. The higher sensitivity of SOM decomposition, and in turn soil respiration, to temperature as compared to net photosynthesis makes investigations into the temperature sensitivity of C mineralization very important (Kirschbaum, 2000, Koch et al., 2007).
The temperature response of SOM decomposition depends upon its molecular structure; recalcitrant compounds have higher activation energies (Ea) than labile and, therefore, theoretically higher temperature sensitivity (Davidson and Janssens, 2006). Yet most existing C models consider a uniform temperature sensitivity of decomposition for organic matter pools of different stabilities (Fierer et al., 2005, Todd-Brown et al., 2012). This issue still needs to be resolved due to variations in findings related to the temperature response of different C pools (Zimmermann and Bird, 2012).
Extracellular enzymes (EE), produced by soil microorganisms, perform the rate-limiting step in SOM decomposition as well as nutrient cycling (Sinsabaugh, 1994, Allison and Vitousek, 2005). Most C models do not take extracellular enzyme kinetics explicitly into consideration (Allison et al., 2010). Recently efforts have been made to develop mechanistic models to simulate the combined effect of temperature, moisture and soluble-substrate supply on soil respiration by considering enzyme kinetics (Davidson et al., 2012). As almost half of the CO2 released from soil is linked to decomposition of SOM by microorganisms and a large fraction of this respired CO2 depends upon EE activity (Ryan and Law, 2005, Frey et al., 2013), adding enzyme kinetics to C models has the potential to improve climate change predictions (Allison et al., 2010).
Environmental factors, such as soil temperature, pH, diffusion constraints, and substrate availability and complexity modify microbial production, expression and temperature sensitivity of EE (Koch et al., 2007, Burns et al., 2013). For example, by analysing samples collected over different seasons from a forest soil Baldrian et al. (2013) found that seasonal variations in soil temperature strongly influenced SOM decomposition by changing the pool size and activity of EE. Different studies have focused on seasonal variations in the temperature sensitivities of soil enzymes (e.g. Koch et al., 2007, Brzostek and Finzi, 2012). However, it is still unclear which factors drive these seasonal trends (Jing et al., 2014). The complex interactions between enzymes and their environment and high variability of their temperature sensitivities makes it impossible to extrapolate single measurements across different temporal scales (Weedon et al., 2011). The current laboratory assays for measuring EE activities are performed under controlled conditions, which do not represent these complex interactions in situ (Henry, 2012). Moreover, this approach neglects the fundamental role of different factors, e.g. temperature and enzyme/substrate diffusion, in controlling in situ enzyme activities (Weedon et al., 2011). To illustrate the interactions of enzyme pool size and seasonal temperature sensitivity patterns in controlling in situ enzyme activities, Wallenstein et al. (2009) developed a predictive model of in situ β-glucosidase activities based on enzyme activities measured at different sampling dates, Q10 and daily soil temperature data from an arctic tundra site.
Little information is available on the effects of soil moisture on the temperature sensitivity of organic matter decomposition (Craine and Gelderman, 2011, Steinweg et al., 2012). Limiting soil moisture can cause a decline in diffusion rates of substrates and, therefore, in EE activity (Davidson and Janssens, 2006). As a consequence, increasing temperatures may not result in a positive feedback to climate change when soil moisture is a limiting factor (Allison and Treseder, 2008). Standard enzyme assays are performed in soil slurry (e.g. Poll et al., 2006, Kramer et al., 2013) for estimating enzyme potentials at non-limiting conditions neglecting diffusion constraint. Recently, Steinweg et al. (2012) developed an assay based on the use of fluorogenic substrates, to account for diffusion limitation at low water content and for non-homogeneous distribution of substrate in soil.
Previous studies have predicted the response of EE activity to in situ temperature and moisture (e.g. Wallenstein et al., 2009, Steinweg et al., 2012) and have yielded valuable insights into soil carbon dynamics. To date, however, the next step, that of using modelled in situ enzyme potentials as an explanatory tool for the seasonal variation of CO2 respiration, is missing.
The goal of the present study is to explore the role of abiotic controls, i.e. soil temperature and moisture, on SOM decomposition by using modelled in situ enzyme activities as a proxy. We modelled in situ temperature-based potentials of three different enzymes (β-glucosidase, xylanase and phenoloxidase) targeting organic matter pools of different complexity, at two different study sites, with and without the presence of vegetation (fallow and vegetation plots). The selection of these three enzymes was based on the assumption that the targeted organic matter pools are representative for most of the soil organic matter pools. We also modelled in situ moisture-based β-glucosidase potential for both study sites and combined both temperature and moisture functions to illustrate the combined effect of both abiotic factors on enzyme potentials. To identify the similarities in seasonal patterns of modelled in situ enzyme activities with soil respiration and to prove the relevance of the modelling approach, we compared the modelled in situ enzyme activities with weekly measured soil surface CO2–C fluxes. We hypothesized that (1) temperature and moisture sensitivity of enzymes targeting organic matter pools of different stability will change during the year. Furthermore, we expected that (2) measured soil CO2 flux correlates strongly with the modelled in situ enzyme potentials, and we expected even stronger correlations with combined controls of soil temperature and moisture on in situ enzyme potentials.
Section snippets
Study site description
We investigated two study regions, with different climatic and edaphic conditions, which are part of the integrated research project “Agricultural landscapes under global climate change – processes and feedbacks on regional scale” (https://klimawandel.uni-hohenheim.de/). The first study site (48°31′7″ N, 9°46′2″ E) is located close to the city of Nellingen in the Swabian Alb region, while the second study site (48°55′7″ N, 8°42′2″ E) is located close to the city of Pforzheim in the Kraichgau
Cmic and potential enzyme activities
Plant input increased microbial biomass C, on average, by 41% in Swabian Alb; in Kraichgau, up to 66% increase was recorded over the whole sampling period (F1,4 = 1188.57 P < 0.01, Fig. S2a and b). Statistical analysis revealed significant seasonal variation in Cmic in the Swabian Alb as well as in the Kraichgau region (F12,96 = 6.51 P < 0.01).
Potential β-glucosidase activity showed significant seasonal (F12,96 = 7.21 P < 0.01) as well as regional (F1,4 = 26.76 P ≤ 0.01) dependence (Fig. 1a and b).
Discussion
Understanding temperature and moisture sensitivity of enzymatic reactions might play an important role in explaining seasonal variation of soil respiration. We found significant seasonal variation in temperature sensitivities of enzymes targeting different substrate pools, which could have important implications for the relative decomposition of SOM and modification of C cycling in predicted climate change scenarios. Seasonal variability in soil temperature was found to be the main controlling
Acknowledgements
This work was supported by the German research foundation (DFG) (KA 1590/10-1) as part of the Research Unit FOR 1695 “Agricultural Landscapes under Global Climate Change – Processes and Feedbacks on a Regional Scale” within project P9. We thank Kathleen Regan for English corrections and we also thank two anonymous reviewers for their constructive comments. We would like to thank the farmers of the Kraichgau and Swabian Alb for providing fields to be used in this study.
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2021, CatenaCitation Excerpt :Soil microbes and enzymes play a key role in the decomposition of SOC. Nearly 50% of the carbon released from the soil is related to the mineralization of SOC by microbes, and a large amount of the respiratory CO2 is related to the activities of soil enzymes (Frey et al., 2013; Ali et al., 2015). An increase in soil temperatures can affect the mineralization of SOC via influences on the biological activity of microorganisms, resulting in the enhancement of enzyme activities that, in turn, lead to a higher rate of decomposition of the soil C pools (Hassan et al., 2015).