Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile

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...

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Autores principales:	Ricardo J. Eloy Alves, Ileana A. Callejas, Gianna L. Marschmann, Maria Mooshammer, Hans W. Singh, Bizuayehu Whitney, Margaret S. Torn, Eoin L. Brodie
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	extracellular enzymes soil subsoil temperature sensitivity Michaelis-Menten Arrhenius Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/981b8fd6913c40288835f1fe26f187c3
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spelling	oai:doaj.org-article:981b8fd6913c40288835f1fe26f187c32021-12-01T18:13:12ZKinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile1664-302X10.3389/fmicb.2021.735282https://doaj.org/article/981b8fd6913c40288835f1fe26f187c32021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.735282/fullhttps://doaj.org/toc/1664-302XCurrent 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.Ricardo J. Eloy AlvesIleana A. CallejasIleana A. CallejasGianna L. MarschmannMaria MooshammerHans W. SinghHans W. SinghBizuayehu WhitneyBizuayehu WhitneyMargaret S. TornMargaret S. TornEoin L. BrodieEoin L. BrodieFrontiers Media S.A.articleextracellular enzymessoilsubsoiltemperature sensitivityMichaelis-MentenArrheniusMicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	extracellular enzymes soil subsoil temperature sensitivity Michaelis-Menten Arrhenius Microbiology QR1-502
spellingShingle	extracellular enzymes soil subsoil temperature sensitivity Michaelis-Menten Arrhenius Microbiology QR1-502 Ricardo J. Eloy Alves Ileana A. Callejas Ileana A. Callejas Gianna L. Marschmann Maria Mooshammer Hans W. Singh Hans W. Singh Bizuayehu Whitney Bizuayehu Whitney Margaret S. Torn Margaret S. Torn Eoin L. Brodie Eoin L. Brodie Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile
description	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.
format	article
author	Ricardo J. Eloy Alves Ileana A. Callejas Ileana A. Callejas Gianna L. Marschmann Maria Mooshammer Hans W. Singh Hans W. Singh Bizuayehu Whitney Bizuayehu Whitney Margaret S. Torn Margaret S. Torn Eoin L. Brodie Eoin L. Brodie
author_facet	Ricardo J. Eloy Alves Ileana A. Callejas Ileana A. Callejas Gianna L. Marschmann Maria Mooshammer Hans W. Singh Hans W. Singh Bizuayehu Whitney Bizuayehu Whitney Margaret S. Torn Margaret S. Torn Eoin L. Brodie Eoin L. Brodie
author_sort	Ricardo J. Eloy Alves
title	Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile
title_short	Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile
title_full	Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile
title_fullStr	Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile
title_full_unstemmed	Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile
title_sort	kinetic properties of microbial exoenzymes vary with soil depth but have similar temperature sensitivities through the soil profile
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/981b8fd6913c40288835f1fe26f187c3
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Kinetic Properties of Microbial Exoenzymes Vary With Soil Depth but Have Similar Temperature Sensitivities Through the Soil Profile

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