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Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities

Predictions concerning the feedback of soil heterotrophic respiration to a warming climate often do not differentiate between the extracellular and intracellular steps involved in soil organic matter decomposition. This study examined the temperature sensitivities of intracellular metabolic processe...

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Published in:Biogeosciences 2023-06, Vol.20 (11), p.2207-2219
Main Authors: Adekanmbi, Adetunji Alex, Dale, Laurence, Shaw, Liz, Sizmur, Tom
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description Predictions concerning the feedback of soil heterotrophic respiration to a warming climate often do not differentiate between the extracellular and intracellular steps involved in soil organic matter decomposition. This study examined the temperature sensitivities of intracellular metabolic processes and extracellular soil enzyme activities and how they are influenced by previous temperatures. We pre-incubated soils at 5, 15, or 26 ∘C to acclimatize the microbial communities to different thermal regimes for 60 d before measuring potential activities of β-glucosidase and chitinase (extracellular enzymes), glucose-induced respiration (intracellular metabolic processes), and basal respiration at a range of assay temperatures (5, 15, 26, 37, and 45 ∘C). A higher pre-incubation temperature decreased the soil pH and C/N ratio and decreased β-glucosidase potential activity and respiration but not chitinase potential activity. It is likely that this legacy effect on β-glucosidase and respiration is an indirect effect of substrate depletion rather than physiological acclimatation or genetic adaptation. Pre-incubation temperature effects on temperature sensitivity were subtle and restricted to extracellular activities, perhaps because of the short (60 d) duration of the pre-incubation at temperatures that were below the initial optimum (∼ 30 ∘C) for the mesophilic soil community. However, we found that the intracellular and extracellular steps differ in their temperature sensitivity, and this observation differs depending on the range of temperature used for Q10 estimates of temperature sensitivity. Between 5 and 15 ∘C intracellular and extracellular processes show equal temperature sensitivity, but between 15 and 26 ∘C intracellular metabolic processes were more temperature sensitive than extracellular enzyme activity, and between 26 and 37 ∘C extracellular enzyme activity was more temperature sensitive than intracellular metabolic processes. This result implies that depolymerization of higher molecular weight carbon is more sensitive to temperature changes at higher temperatures (e.g. higher temperatures on extremely warm days), but the respiration of the generated monomers is more sensitive to temperature changes at moderate temperatures (e.g. mean daily maximum soil temperature). However, studies using multiple soil types and a greater range of pre-incubation temperatures are required to generalize our results. Nevertheless, since climate change predictions curr
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This study examined the temperature sensitivities of intracellular metabolic processes and extracellular soil enzyme activities and how they are influenced by previous temperatures. We pre-incubated soils at 5, 15, or 26 ∘C to acclimatize the microbial communities to different thermal regimes for 60 d before measuring potential activities of β-glucosidase and chitinase (extracellular enzymes), glucose-induced respiration (intracellular metabolic processes), and basal respiration at a range of assay temperatures (5, 15, 26, 37, and 45 ∘C). A higher pre-incubation temperature decreased the soil pH and C/N ratio and decreased β-glucosidase potential activity and respiration but not chitinase potential activity. It is likely that this legacy effect on β-glucosidase and respiration is an indirect effect of substrate depletion rather than physiological acclimatation or genetic adaptation. Pre-incubation temperature effects on temperature sensitivity were subtle and restricted to extracellular activities, perhaps because of the short (60 d) duration of the pre-incubation at temperatures that were below the initial optimum (∼ 30 ∘C) for the mesophilic soil community. However, we found that the intracellular and extracellular steps differ in their temperature sensitivity, and this observation differs depending on the range of temperature used for Q10 estimates of temperature sensitivity. Between 5 and 15 ∘C intracellular and extracellular processes show equal temperature sensitivity, but between 15 and 26 ∘C intracellular metabolic processes were more temperature sensitive than extracellular enzyme activity, and between 26 and 37 ∘C extracellular enzyme activity was more temperature sensitive than intracellular metabolic processes. This result implies that depolymerization of higher molecular weight carbon is more sensitive to temperature changes at higher temperatures (e.g. higher temperatures on extremely warm days), but the respiration of the generated monomers is more sensitive to temperature changes at moderate temperatures (e.g. mean daily maximum soil temperature). However, studies using multiple soil types and a greater range of pre-incubation temperatures are required to generalize our results. Nevertheless, since climate change predictions currently indicate that there will be a greater frequency and severity of hot summers and heatwaves, it is possible that global warming may reduce the importance of extracellular depolymerization relative to intracellular metabolic processes as the rate-limiting step of soil organic matter mineralization. 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This study examined the temperature sensitivities of intracellular metabolic processes and extracellular soil enzyme activities and how they are influenced by previous temperatures. We pre-incubated soils at 5, 15, or 26 ∘C to acclimatize the microbial communities to different thermal regimes for 60 d before measuring potential activities of β-glucosidase and chitinase (extracellular enzymes), glucose-induced respiration (intracellular metabolic processes), and basal respiration at a range of assay temperatures (5, 15, 26, 37, and 45 ∘C). A higher pre-incubation temperature decreased the soil pH and C/N ratio and decreased β-glucosidase potential activity and respiration but not chitinase potential activity. It is likely that this legacy effect on β-glucosidase and respiration is an indirect effect of substrate depletion rather than physiological acclimatation or genetic adaptation. Pre-incubation temperature effects on temperature sensitivity were subtle and restricted to extracellular activities, perhaps because of the short (60 d) duration of the pre-incubation at temperatures that were below the initial optimum (∼ 30 ∘C) for the mesophilic soil community. However, we found that the intracellular and extracellular steps differ in their temperature sensitivity, and this observation differs depending on the range of temperature used for Q10 estimates of temperature sensitivity. Between 5 and 15 ∘C intracellular and extracellular processes show equal temperature sensitivity, but between 15 and 26 ∘C intracellular metabolic processes were more temperature sensitive than extracellular enzyme activity, and between 26 and 37 ∘C extracellular enzyme activity was more temperature sensitive than intracellular metabolic processes. This result implies that depolymerization of higher molecular weight carbon is more sensitive to temperature changes at higher temperatures (e.g. higher temperatures on extremely warm days), but the respiration of the generated monomers is more sensitive to temperature changes at moderate temperatures (e.g. mean daily maximum soil temperature). However, studies using multiple soil types and a greater range of pre-incubation temperatures are required to generalize our results. Nevertheless, since climate change predictions currently indicate that there will be a greater frequency and severity of hot summers and heatwaves, it is possible that global warming may reduce the importance of extracellular depolymerization relative to intracellular metabolic processes as the rate-limiting step of soil organic matter mineralization. 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subjects Acclimatization
Adaptation
Carbon/nitrogen ratio
Chitinase
Climate change
Climate prediction
Decomposition
Depolymerization
Enzymatic activity
Enzyme activity
Enzymes
Extracellular enzymes
Global warming
Glucose
Glucosidase
Heat waves
Heatwaves
Hot summers
Incubation period
Intracellular
Metabolism
Microbial activity
Microorganisms
Mineralization
Moisture content
Molecular weight
Monomers
Observatories
Organic matter
Organic soils
Physiological aspects
Physiological effects
Respiration
Sensitivity
Soil
Soil chemistry
Soil organic matter
Soil pH
Soil temperature
Soil types
Substrates
Temperature
Temperature changes
Temperature effects
β-Glucosidase
title Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities
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