Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities
<p>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...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Copernicus Publications
2023-06-01
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| Series: | Biogeosciences |
| Online Access: | https://bg.copernicus.org/articles/20/2207/2023/bg-20-2207-2023.pdf |
| _version_ | 1797802500739301376 |
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| author | A. A. Adekanmbi A. A. Adekanmbi L. Dale L. Shaw T. Sizmur |
| author_facet | A. A. Adekanmbi A. A. Adekanmbi L. Dale L. Shaw T. Sizmur |
| author_sort | A. A. Adekanmbi |
| collection | DOAJ |
| description | <p>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 <span class="inline-formula"><sup>∘</sup></span>C to acclimatize the
microbial communities to different thermal regimes for 60 d before
measuring potential activities of <span class="inline-formula"><i>β</i></span>-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 <span class="inline-formula"><sup>∘</sup></span>C). A higher pre-incubation temperature
decreased the soil pH and <span class="inline-formula"><math xmlns="http://www.w3.org/1998/Math/MathML" id="M4" display="inline" overflow="scroll" dspmath="mathml"><mrow class="chem"><mi mathvariant="normal">C</mi><mo>/</mo><mi mathvariant="normal">N</mi></mrow></math><span><svg:svg xmlns:svg="http://www.w3.org/2000/svg" width="24pt" height="14pt" class="svg-formula" dspmath="mathimg" md5hash="a1fd226718b6fd2378e4d645ff1b8807"><svg:image xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="bg-20-2207-2023-ie00001.svg" width="24pt" height="14pt" src="bg-20-2207-2023-ie00001.png"/></svg:svg></span></span> ratio and decreased <span class="inline-formula"><i>β</i></span>-glucosidase potential
activity and respiration but not chitinase potential activity. It is likely
that this legacy effect on <span class="inline-formula"><i>β</i></span>-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
(<span class="inline-formula">∼</span> 30 <span class="inline-formula"><sup>∘</sup></span>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 <span class="inline-formula"><i>Q</i><sub>10</sub></span> estimates of temperature sensitivity.
Between 5 and 15 <span class="inline-formula"><sup>∘</sup></span>C intracellular and extracellular processes show equal temperature sensitivity, but between 15 and 26 <span class="inline-formula"><sup>∘</sup></span>C intracellular metabolic processes were
more temperature sensitive than extracellular enzyme activity, and between 26 and 37 <span class="inline-formula"><sup>∘</sup></span>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. We conclude that extracellular and intracellular steps are
not equally sensitive to changes in soil temperature and that the previous
temperature a soil is exposed to may influence the potential activity, but
not temperature sensitivity, of extracellular and intracellular processes.</p> |
| first_indexed | 2024-03-13T05:07:42Z |
| format | Article |
| id | doaj.art-2ef4e07689c44a6ebad1b139167e1256 |
| institution | Directory Open Access Journal |
| issn | 1726-4170 1726-4189 |
| language | English |
| last_indexed | 2024-03-13T05:07:42Z |
| publishDate | 2023-06-01 |
| publisher | Copernicus Publications |
| record_format | Article |
| series | Biogeosciences |
| spelling | doaj.art-2ef4e07689c44a6ebad1b139167e12562023-06-16T07:00:22ZengCopernicus PublicationsBiogeosciences1726-41701726-41892023-06-01202207221910.5194/bg-20-2207-2023Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activitiesA. A. Adekanmbi0A. A. Adekanmbi1L. Dale2L. Shaw3T. Sizmur4Department of Geography and Environmental Science, University of Reading, Reading, RG6 6DW, UKDepartment of Soil Science and Land Management, Federal University of Technology, PMB 65, 920001, Minna, NigeriaDepartment of Geography and Environmental Science, University of Reading, Reading, RG6 6DW, UKDepartment of Geography and Environmental Science, University of Reading, Reading, RG6 6DW, UKDepartment of Geography and Environmental Science, University of Reading, Reading, RG6 6DW, UK<p>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 <span class="inline-formula"><sup>∘</sup></span>C to acclimatize the microbial communities to different thermal regimes for 60 d before measuring potential activities of <span class="inline-formula"><i>β</i></span>-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 <span class="inline-formula"><sup>∘</sup></span>C). A higher pre-incubation temperature decreased the soil pH and <span class="inline-formula"><math xmlns="http://www.w3.org/1998/Math/MathML" id="M4" display="inline" overflow="scroll" dspmath="mathml"><mrow class="chem"><mi mathvariant="normal">C</mi><mo>/</mo><mi mathvariant="normal">N</mi></mrow></math><span><svg:svg xmlns:svg="http://www.w3.org/2000/svg" width="24pt" height="14pt" class="svg-formula" dspmath="mathimg" md5hash="a1fd226718b6fd2378e4d645ff1b8807"><svg:image xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="bg-20-2207-2023-ie00001.svg" width="24pt" height="14pt" src="bg-20-2207-2023-ie00001.png"/></svg:svg></span></span> ratio and decreased <span class="inline-formula"><i>β</i></span>-glucosidase potential activity and respiration but not chitinase potential activity. It is likely that this legacy effect on <span class="inline-formula"><i>β</i></span>-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 (<span class="inline-formula">∼</span> 30 <span class="inline-formula"><sup>∘</sup></span>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 <span class="inline-formula"><i>Q</i><sub>10</sub></span> estimates of temperature sensitivity. Between 5 and 15 <span class="inline-formula"><sup>∘</sup></span>C intracellular and extracellular processes show equal temperature sensitivity, but between 15 and 26 <span class="inline-formula"><sup>∘</sup></span>C intracellular metabolic processes were more temperature sensitive than extracellular enzyme activity, and between 26 and 37 <span class="inline-formula"><sup>∘</sup></span>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. We conclude that extracellular and intracellular steps are not equally sensitive to changes in soil temperature and that the previous temperature a soil is exposed to may influence the potential activity, but not temperature sensitivity, of extracellular and intracellular processes.</p>https://bg.copernicus.org/articles/20/2207/2023/bg-20-2207-2023.pdf |
| spellingShingle | A. A. Adekanmbi A. A. Adekanmbi L. Dale L. Shaw T. Sizmur Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities Biogeosciences |
| title | Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities |
| title_full | Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities |
| title_fullStr | Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities |
| title_full_unstemmed | Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities |
| title_short | Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities |
| title_sort | differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities |
| url | https://bg.copernicus.org/articles/20/2207/2023/bg-20-2207-2023.pdf |
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