Eurasian Soil ScienceEurasian Soil Science0032-180X3034-5618Russian Academy of Science10.31857/S0032180X2260130XEffect of Long-Term and Short-Term Droughts on the Hydrolytic Enzymes in Haplic LuvisolВлияние длительной и кратковременных засух на гидролитические ферменты серой почвыhttps://orcid.org/0000-0002-4058-2549YakushevA. V.ЯкушевА. В. a_yakushev84@mail.ruООО “Агро-С”LLC “Agro-S”010620236745757

The transformation of organic matter in the soil is largely determined by hydrolytic enzymes. Under the conditions of climate change, understanding the mechanisms of microbial response is of particular importance for predicting the carbon cycle. Until now, the effect of drought duration and frequency on soil hydrolytic enzymes has been little studied. A multifactorial field manipulation experiment was carried out, simulating in the presence of plants and without them: two short-term droughts, a long-term drought, and an optimal level of soil moisture. The maximum reaction rate Vmax, Michaelis constant Km, and catalytic efficiency Ka of five groups of enzymes involved in the carbon cycle (cellobiase, glucosidase, xylanase), phosphorus (phosphatase), and nitrogen (chitinase) were determined. In phosphatases, glucosidases, and xylanases, Vmax decreased during short-term drought. During prolonged drought, the Vmax value of phosphatases, cellobiohydrolases, and xylanases decreased and increased in chitinases, while remaining unchanged in glucosidases. Both long-term and short-term droughts led to an increase in Km and a decrease in catalytic efficiency (Ka) for almost all enzymes. Short-term droughts were not a “weakened version” of a long-term drought, but had their own specifics – a decrease in Km in glucosidases, which led to an increase in Ka. Long-term drought was characterized by an increase in Vmax of chitinases and spatial variability of Vmax of phosphatases and glucosidases. The influence of the presence of plants was secondary and affected only during short droughts. The reversibility of the effect of drought on Vmax, Km, Ka decreased in the series first short-term drought > second short-term drought > long-term drought due to an increase in the total duration of the stress impact.

Трансформация органического вещества в почве во многом определяется гидролитическими ферментами. В условиях климатических изменений особенное значение имеет понимание механизмов микробного отклика для прогнозирования цикла углерода. До сих пор мало изучалось влияние продолжительности и частоты засухи на гидролитические ферменты почвы. Проведен многофакторный полевой манипуляционный эксперимент, моделирующий в присутствии растений и без них: две кратковременные засухи, длительную засуху и оптимальный уровень увлажнения почвы. Определяли максимальную скорость реакции Vmax, константу Михаэлиса Km и каталитическую эффективность Ka пяти групп ферментов, участвующих в цикле углерода (целлобиазы, глюкозидазы, ксиланазы), фосфора (фосфатазы) и азота (хитиназы). У фосфатаз, глюкозидаз и ксиланаз Vmax снижалось при кратковременной засухе. В ходе длительной засухи снижалось значение Vmax фосфатаз, целлобиогидролаз, ксиланаз и возрастало у хитиназ, оставаясь при этом неизменным у глюкозидаз. Как длительная, так и кратковременные засухи приводили к увеличению Km и уменьшению Ka почти для всех ферментов. Кратковременные засухи не являлись ослабленным вариантом длительной засухи, но имели свою специфику – снижение у глюкозидаз Km, которое приводило к увеличению Kа. Длительная засуха отличалась увеличением Vmax хитиназ и пространственной вариативности Vmax фосфатаз и глюкозидаз. Влияние присутствия растений было второстепенным и сказывалось только при коротких засухах. Обратимость действия засухи на Vmax, Km, Ka уменьшалась в ряду: первая кратковременная засуха > вторая кратковременная засуха > длительная засуха – за счет увеличения общей продолжительности стрессового воздействия.

почвенная засуха почвенные ферменты кинетика Михаэлиса–Ментен каталитическая эффективность ферментовпочвенная засуха почвенные ферменты кинетика Михаэлиса–Ментен каталитическая эффективность ферментовАвторы статьи благодарят к. б. н. Е.В. Благодатскую, к. б. н., В.О. Лопеса де Гереню и к. б. н. И.В. Евдокимова за помощь в работе.Авторы статьи благодарят к. б. н. Е.В. Благодатскую, к. б. н., В.О. Лопеса де Гереню и к. б. н. И.В. Евдокимова за помощь в работе.Овсепян Л.А., Курганова И.Н., Мостовая А.С., Лопес де Гереню. В.О., Личко В.И., Благодатская Е.В., Кузяков Я.В. Ферментативная активность пост-агрогенных серых лесных почв нагорной дубравы “Лес на Ворскле” // Известия Самарского научного центра РАН. 2017. Т. 19. № 2. С. 151–158.Семенов В.М., Лебедева Т.Н., Зинякова Н.Б., Хромычкина Д.П., Соколов Д.А., Лопес де Гереню В.О., Кравченко И.К., Ли Х., Семенов М.В. Зависимость разложения органического вещества почвы и растительных остатков от температуры и влажности в длительных инкубационных экспериментах // Почвоведение. 2022. № 7. С. 860–875. https://doi.org/10.31857/S0032180X22070085Alves R.J., Callejas I.A., Marschmann G., Mooshammer M., Singh H.W., Whitney B., Torn M.S., Brodie E.L. Kinetic Properties of Microbial Exoenzymes Vary with Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile // Frontiers in Microbiology. 2021. V. 12. P. 735282. https://doi.org/10.3389/fmicb.2021.735282Baker N.R., Allison S.D. Extracellular enzyme kinetics and thermodynamics along a climate gradient in Southern California // Soil Biol. Biochem. 2017. V. 114. P. 82–92. https://doi.org/10.1016/j.soilbio.2017.07.005Barnard R.L., Osborne C.A., Firestone M.K. Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate // Int. Soc. Microbial Ecology. 2014. V. 9. P. 946–957. https://doi.org/10.1038/ismej.2014.192Burns R.G., DeForest J.L., Marxsen J., Sinsabaugh R.L., Stromberger M.E., Wallenstein M.D., Weintraub M.N., Zoppini A. Soil enzymes in a changing environment: Current knowledge and future directions // Soil Biol. Biochem. 2013 V. 58. P. 216–234. https://doi.org/10.1016/j.soilbio.2012.11.009Davidson E., Janssens I. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change // Nature. 2006. V. 440. P. 165–173. https://doi.org/10.1038/nature04514Dick R.P., Sandor J.A., Eash N.S. Soil enzyme activities after 1500 years of terrace agriculture in the Colca Valley, Peru // Agriculture, Ecosystems & Environment. 1994. V. 50. P. 123–131. https://doi.org/10.1016/0167-8809(94)90131-7German D.P., Marcelo K.R.B., Stone M.M., Allison S.D. The Michaelis–Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study // Global Change Biol. 2012. V. 18. P. 1468–1479. https://doi.org/10.1111/j.1365-2486.2011.02615.xGianfreda L., Rao M.A., Piotrowska A., Palumbo G., Colombo C. Soil enzyme activities as affected by anthropogenic alterations: intensive agricultural practices and organic pollution // Sci. Total Environ. 2005. V. 341. I. 1–3. P. 265–279. https://doi.org/10.1016/j.scitotenv.2004.10.005IPCC C. W. T. Climate Change 2007: Synthesis Report. Geneva, Switzerland IPCC, 2007. P. 104.Juan Y., Chen L., Wu Z.J., Wang R. Kinetics of soil urease affected by urease inhibitors at contrasting moisture regimes // J. Soil Sci. Plant Nutrition. 2009. V. 9. P. 125–133.Khalili B., Nourbakhsh F., Nili N., Khademi H., Sharifnabi B. Diversity of soil cellulase isoenzymes is associated with soil cellulose kinetic and thermodynamic parameters // Soil Biol. Biochem. 2011. V. 43. P. 1639–1648.Kovárová–Kovar K., Egli T. Growth Kinetics of Suspended Microbial Cells: From Single-Substrate-Controlled Growth to Mixed-Substrate Kinetics // Microbiol. Molecular Biol. Rev. 1998. V. 62. P. 646–666.Kujur M., Patel A.K. Kinetics of soil enzyme activities under different ecosystems: An index of soil quality // Chilean J. Agricult.Res. 2014. V. 74. P. 96–104. https://doi.org/10.4067/S0718-58392014000100015Loeppmann S., Blagodatskaya E., Pausch J., Kuzyakov Y. Substrate quality affects kinetics and catalytic efficiency of exoenzymes in rhizosphere and detritusphere // Soil Biol. Biochem. 2016. V. 92. P. 111–118.von Lützow M., Kogel-Knabner I. Temperature Sensitivity of Soil Organic Matter Decomposition – What Do We Know? // Biol. Fertil. Soils. 2009. V. 46. P. 1–15. https://doi.org/10.1007/s00374-009-0413-8Liu C., Tian H., Gu X., Li N., Zhao X., Lei M., Alharbi H., Megharaj M., He W., Kuzyakov Y. Catalytic efficiency of soil enzymes explains temperature sensitivity: Insights from physiological theory // Sci. Total Environ. V. 822. 2022. P. 153365. https://doi.org/10.1016/j.scitotenv.2022.153365Marx M.C., Wood M., Jarvis S.C. A microplate fluorimetric assay for the study of enzyme diversity in soils // Soil Biol. Biochem. 2001. V. 33. P. 1633–1640.Marx M., Kandeler E., Wood M.K., Wermbter N., Jarvis S.C. Exploring the enzymatic landscape: distribution and kinetics of hydrolytic enzymes in soil particle-size fractions // Soil Biol. Biochem. 2005. V. 37. P. 35–48.Moscatelli M.C., Lagomarsino A., Garzillo A.M.V., Pignataro A., Grego S. Glucosidase kinetic parameters as indicators of soil quality under conventional and organic cropping systems applying two analytical approaches // Ecological Indicators. 2012. V. 13. P. 322–327.Nannipieri P., Grego S., Ceccanti B. Ecological significance of the biological activity in soil // Soil Biochem. 1990. V. 6. P. 293–355.Sanaullah M., Blagodatskaya E., Chabbi A., Rumpel C., Kuzyakov Y. Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition // Appl. Soil Ecology. 2011. V. 48. P. 38–44.Schimel J. Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes // Ann. Rev. Ecology, Evolution, Systematics. 2018 V. 49. P. 409–432.Schneider T., Keiblinger K.M., Schmid E., Sterflinger–Gleixner K., Ellersdorfer G., Roschitzki B., Richter A., Eberl L., Zechmeister–Boltenstern S., Riedel K. Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions // The ISME J. 2012. V. 6. P. 1749–1762.Skujins J. Extracellular enzymes in soil // Critical Rev. Microbiol. 1976. V. 44. P. 383–421.Steinweg J.M. Sensitivity of microbial community physiology to soil moisture and temperature in an old field ecosystem. Doctoral dissertation, 2011.Stone M.M., Weiss M.S., Goodale C.L., Adams M.B., Fernandez I.J., German D.P., Allison S.D. Temperature sensitivity of soil enzyme kinetics under N-fertilization in two temperate forests // Global Change Biol. 2012. V. 18. P. 1173–1184.Stursova M., Baldrian P. Effects of soil properties and management on the activity of soil organic matter transforming enzymes and the quantification of soil-bound and free activity // Plant Soil. 2011. V. 338. P. 99–110.Tischer A., Blagodatskaya E., Hamer U. Microbial community structure and resource availability drive the catalytic efficiency of soil enzymes under land-use change conditions // Soil Biol. Biochem. 2015. V. 89. P. 226–237.Wallenstein M.D., McMahon S.K., Schimel J.P. Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils // Global Change Biol. 2009. V. 15. P. 1631–1639.Wang G., Post W.M., Mayes M.A., Frerichs J.T., Sindhu J. Parameter estimation for models of ligninolytic and cellulolytic enzyme kinetics // Soil Biol. Biochem. 2012. V. 48. P. 28–38.Zhang Y., Chen L., Wu Z., Sun C. Kinetic parameters of soil β-glucosidase response to environmental temperature and moisture regimes // Revista Brasileira De Ciencia Do Solo. 2011. V. 35. P. 1285–1291.Yuste J.C., Barba J., Fernández-González A.J., Fernández–López M., Mattana S., Martínez–Vilalta J., Nolis P., Lloret F. Changes in soil bacterial community triggered by drought-induced gap succession preceded changes in soil C stocks and quality // Ecology Evolution. 2012. V. 2. P. 3016–3031.