Soil Enzyme Kinetics, Temperature Sensitivity and the Response of Soil Enzymes to Tillage and Conservation-Based Management: A Review
Abstract
Soil enzymes mediate the breakdown of organic matter and the release of carbon, nitrogen and phosphorus, and their activity is widely used as an early indicator of changes in soil quality. Interpreting that activity, however, requires an understanding of both the kinetics of the enzymes themselves and the environmental and management conditions under which they operate. This narrative review draws together recent studies and reviews on three linked themes: the kinetic description of enzyme-catalyzed reactions and the way pH, temperature and inhibitors modify it; the temperature sensitivity of soil enzymes and its consequences for nutrient stoichiometry; and the response of enzyme activities to tillage, residue retention and climate-smart cropping systems, including the role of dehydrogenase as an indicator of microbial function. The evidence shows that kinetic parameters measured in soil are apparent rather than intrinsic, that temperature sensitivity differs strongly among enzyme groups and can fall below the commonly assumed Q10 of 2, and that reduced tillage and residue retention generally raise soil organic carbon, microbial biomass and the activity of many hydrolytic enzymes, although not all enzymes respond and the relationships between enzymes and environmental factors change with management. Most field studies report potential activity from a single site and season and do not measure kinetic parameters, which limits mechanistic interpretation. Studies that combine kinetic parameters, temperature responses and management treatments across seasons are needed.
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Introduction
Most of the organic matter in soil is present as polymers that microorganisms cannot take up directly. Microbes therefore release enzymes that depolymerize this material into soluble oligomers and monomers, which are then transported into the cell (Wallenstein et al., 2011). Enzymes that release glucose, amino acids and phosphate, such as β-glucosidase, aminopeptidases and phosphatases, sit at the interface between soil organic matter and microbial nutrition, and their activity influences both nutrient availability and the fate of carbon. Because enzyme activity responds to disturbance and to changes in management sooner than many bulk soil properties, it has been proposed as a sensitive indicator of soil quality (Pandey et al., 2015; Jat et al., 2021).
At the same time, agricultural systems are being redesigned to produce more food with less degradation of the soil. Conservation agriculture (CA) is one such approach. It combines minimum or no tillage with permanent soil cover and diversified crop rotations that include legumes, and it is promoted as a means of maintaining soil organic carbon and soil function (Page et al., 2020). Page et al. (2020) concluded that the effect of CA on soil organic carbon varies among regions, but that where conditions favor biomass production and yields are not penalized, CA generally leads to higher organic carbon near the soil surface, often accompanied by better soil structure and greater microbial biomass and diversity. Enzyme activities are a natural way to probe whether these changes in organic carbon also translate into changes in biological function.
Two bodies of research address enzymes in soil, and they are often reported separately. Biochemical and ecological studies describe how fast enzyme-catalyzed reactions proceed and why, using the language of kinetic parameters and activation energies (Ahenkorah et al., 2021; Wallenstein et al., 2011; Bárta et al., 2013). Agronomic studies compare enzyme activities among tillage systems, cropping systems and land uses (Pandey et al., 2015; Jat et al., 2021; Kumar et al., 2013). The purpose of this review is to bring these two perspectives together. We first set out the kinetic framework and the factors that modify it, then examine temperature sensitivity, then summarize evidence on tillage and conservation-based management, and finally consider dehydrogenase as a general indicator. We close by identifying the main limitations of current evidence and the research needed to link kinetics with management. The review is based mainly on six recent studies and reviews (Table 1), supplemented by earlier work cited within them and clearly attributed where used.
Conclusion
Enzyme kinetics offers a quantitative way of separating the effects of enzyme quantity, substrate affinity and environmental modifiers such as pH, temperature and inhibitors, but parameters measured in soil are apparent ones and must be interpreted with care. Temperature sensitivity is enzyme-specific and context-dependent: in an acidic forest soil, hydrolytic enzymes for carbon and phosphorus warmed as expected whereas aminopeptidases did not, with consequences for modeled nutrient release. Reduced tillage and residue-retaining systems generally raise soil organic carbon, microbial biomass and the activity of many carbon-, nitrogen- and phosphorus-cycling enzymes, but not all enzymes respond, and the relationships between enzymes and environmental variables change with management. Dehydrogenase remains a useful but method-sensitive indicator of overall microbial function in disturbed and natural soils. Linking these strands will require studies that measure kinetic parameters directly in managed soils across seasons, using standardized methods.
References
- Ahenkorah, I., Rahman, M. M., Karim, M. R., Beecham, S., & Saint, C. (2021). A review of enzyme induced carbonate precipitation (EICP): The role of enzyme kinetics. Sustainable Chemistry, *2*, 92-114. https://doi.org/10.3390/suschem2010007
- Allen, A. P., & Gillooly, J. F. (2009). Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecology Letters, *12*, 369-384.
- Bárta, J., Šlajsová, P., Tahovská, K., Picek, T., & Šantrůčková, H. (2013). Different temperature sensitivity and kinetics of soil enzymes indicate seasonal shifts in C, N and P nutrient stoichiometry in acid forest soil. Biogeochemistry. https://doi.org/10.1007/s10533-013-9898-1
- Casida, L. E., Jr., Klein, D. A., & Santoro, T. (1964). Soil dehydrogenase activity. Soil Science, *98*, 371-376.
- Choudhary, M., Jat, H. S., Datta, A., Yadav, A. K., Sapkota, T. B., Mondal, S., et al. (2018). Sustainable intensification influences soil quality, biota, and productivity in cereal-based agroecosystems. Applied Soil Ecology, *126*, 189-198.
- Chróst, R. G. (1990). Microbial ectoenzymes in aquatic environments. In J. Overbeck & R. J. Chróst (Eds.), Aquatic microbial ecology: Biochemical and molecular approaches (pp. 47-78). Springer.
- Davidson, E. A., & Janssens, I. A. (2006). Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature, *440*, 165-173.
- Dick, W. A. (1994). Influence of long-term tillage and crop rotation combinations on soil enzyme activities. Soil Science Society of America Journal, *56*, 783-788.
- Fidaleo, M., & Lavecchia, R. (2003). Kinetic study of enzymatic urea hydrolysis in the pH range 4–9. Chemical and Biochemical Engineering Quarterly, *17*, 311-318.
- Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M., & Charnov, E. L. (2001). Effects of size and temperature on metabolic rate. Science, *293*, 2248-2251.
- Hinojosa, M. B., García-Ruiz, R., Viñegla, B., & Carreira, J. A. (2004). Microbiological rates and enzyme activities as indicators of functionality in soils affected by the Aznalcóllar toxic spill. Soil Biology and Biochemistry, *36*, 1637-1644.
- Jat, H. S., Datta, A., Choudhary, M., Sharma, P. C., Dixit, B., & Jat, M. L. (2021). Soil enzymes activity: Effect of climate smart agriculture on rhizosphere and bulk soil under cereal based systems of north-west India. European Journal of Soil Biology, *103*, 103292. https://doi.org/10.1016/j.ejsobi.2021.103292
- Krajewska, B. (2009). Ureases I. Functional, catalytic and kinetic properties: A review. Journal of Molecular Catalysis B: Enzymatic, *59*, 9-21.
- Kumar, S., Chaudhuri, S., & Maiti, S. K. (2013). Soil dehydrogenase enzyme activity in natural and mine soil – A review. Middle East Journal of Scientific Research, *13*, 898-906. https://doi.org/10.5829/idosi.mejsr.2013.13.7.2801
- Kuzyakov, Y. (2002). Review: Factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science, *165*, 382-396.
- Marx, M. C., Wood, M., & Jarvis, S. C. (2001). A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biology and Biochemistry, *33*, 1633-1640.
- Michaelis, L., & Menten, M. L. (1913). Die Kinetik der Invertinwirkung. Biochemische Zeitschrift, *49*, 333-369.
- Page, K. L., Dang, Y. P., & Dalal, R. C. (2020). The ability of conservation agriculture to conserve soil organic carbon and the subsequent impact on soil physical, chemical, and biological properties and yield. Frontiers in Sustainable Food Systems, *4*, 31. https://doi.org/10.3389/fsufs.2020.00031
- Pandey, D., Agrawal, M., & Bohra, J. S. (2015). Assessment of soil quality under different tillage practices during wheat cultivation: Soil enzymes and microbial biomass. Chemistry and Ecology, *31*, 510-523. https://doi.org/10.1080/02757540.2015.1029462
- Pausch, J., & Kuzyakov, Y. (2018). Carbon input by roots into the soil: Quantification of rhizodeposition from root to ecosystem scale. Global Change Biology, *24*, 1-12.
- Puglisi, E., Del Re, A. A. M., Rao, M. A., & Gianfreda, L. (2006). Development and validation of numerical indexes integrating enzyme activities of soils. Soil Biology and Biochemistry, *38*, 1673-1681.
- Sinsabaugh, R. L. (2010). Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biology and Biochemistry, *42*, 391-404.
- Sinsabaugh, R. L., Hill, B. H., & Follstad Shah, J. J. (2009). Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature, *462*, 795-799.
- Stayton, M. M., & Fromm, H. J. (1979). A computer analysis of the validity of the integrated Michaelis–Menten equation. Journal of Theoretical Biology, *78*, 309-323.
- Steinweg, J. M., Jagadamma, S., Frerichs, J., & Mayes, M. A. (2013). Activation energy of extracellular enzymes in soils from different biomes. PLoS ONE, *8*, e59943.
- Trasar-Cepeda, C., Gil-Sotres, F., & Leirós, M. C. (2007). Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain. Soil Biology and Biochemistry, *39*, 311-319.
- Trevors, J. T. (1984). Dehydrogenase activity in soil: A comparison between the INT and TTC assay. Soil Biology and Biochemistry, *16*, 673-674.
- Von Mersi, W., & Schinner, F. (1991). An improved and accurate method for determining the dehydrogenase activity of soils with iodonitrotetrazolium chloride. Biology and Fertility of Soils, *11*, 216-220.
- Wallenstein, M., Allison, S. D., Ernakovich, J., Steinweg, J. M., & Sinsabaugh, R. (2011). Controls on the temperature sensitivity of soil enzymes: A key driver of in situ enzyme activity rates. In G. Shukla & A. Varma (Eds.), Soil enzymology (pp. 245-258). Springer. https://doi.org/10.1007/978-3-642-14225-3_13
- Wallenstein, M. D., McMahon, S. K., & Schimel, J. P. (2009). Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Global Change Biology, *15*, 1631-1639.