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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 |
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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 |
doi_str_mv | 10.5194/bg-20-2207-2023 |
format | article |
fullrecord | <record><control><sourceid>gale_doaj_</sourceid><recordid>TN_cdi_doaj_primary_oai_doaj_org_article_2ef4e07689c44a6ebad1b139167e1256</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A753193260</galeid><doaj_id>oai_doaj_org_article_2ef4e07689c44a6ebad1b139167e1256</doaj_id><sourcerecordid>A753193260</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3463-b515e385fd286ef67a4604a128de4811922ea2fbc3255dddfce4cdd0dcf213463</originalsourceid><addsrcrecordid>eNptks2L1TAQwIsouK6evQY8eehuvtqmx2V19cGC4Mc5TJNJyaNtnkkqPv96032i-0BymDD85kdmMlX1mtGrhvXyehhrTmvOaVciF0-qC9bxtpZM9U8f3Z9XL1LaUyoUVc1FFd955zDikj1MJON8wAh5jUgSLsln_8PnIwmO-CVHMDhN6wSRzJhhCJM35BCDwZQwEVgswZ-PqRT8RHD5dZyRgHlweUwvq2cOpoSv_sTL6tvd-6-3H-v7Tx92tzf3tRGyFfXQsAaFapzlqkXXdiBbKoFxZVEqxnrOEbgbjOBNY611BqWxllrjONsMl9Xu5LUB9voQ_QzxqAN4_ZAIcdQQszcTao5OIu1a1RspocUBLBuY6FnbIePN5npzcpV2v6-Yst6HNS7l-Zor3tLyA4r_o0YoUr-4sE1j9snom64RrBcFLdTVf6hyLM7ehAWdL_mzgrdnBYXJZdAjrCnp3ZfP5-z1iTUxpBTR_W2cUb3tiR5Gzane9kRveyJ-A-2RsK4</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2826051982</pqid></control><display><type>article</type><title>Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities</title><source>Publicly Available Content Database</source><source>DOAJ Directory of Open Access Journals</source><creator>Adekanmbi, Adetunji Alex ; Dale, Laurence ; Shaw, Liz ; Sizmur, Tom</creator><creatorcontrib>Adekanmbi, Adetunji Alex ; Dale, Laurence ; Shaw, Liz ; Sizmur, Tom</creatorcontrib><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
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.</description><identifier>ISSN: 1726-4189</identifier><identifier>ISSN: 1726-4170</identifier><identifier>EISSN: 1726-4189</identifier><identifier>DOI: 10.5194/bg-20-2207-2023</identifier><language>eng</language><publisher>Katlenburg-Lindau: Copernicus GmbH</publisher><subject>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</subject><ispartof>Biogeosciences, 2023-06, Vol.20 (11), p.2207-2219</ispartof><rights>COPYRIGHT 2023 Copernicus GmbH</rights><rights>2023. This work is published under https://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3463-b515e385fd286ef67a4604a128de4811922ea2fbc3255dddfce4cdd0dcf213463</cites><orcidid>0000-0001-9835-7195 ; 0000-0003-3379-4161</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2826051982/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2826051982?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,864,2102,25753,27924,27925,37012,44590,75126</link.rule.ids></links><search><creatorcontrib>Adekanmbi, Adetunji Alex</creatorcontrib><creatorcontrib>Dale, Laurence</creatorcontrib><creatorcontrib>Shaw, Liz</creatorcontrib><creatorcontrib>Sizmur, Tom</creatorcontrib><title>Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities</title><title>Biogeosciences</title><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
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.</description><subject>Acclimatization</subject><subject>Adaptation</subject><subject>Carbon/nitrogen ratio</subject><subject>Chitinase</subject><subject>Climate change</subject><subject>Climate prediction</subject><subject>Decomposition</subject><subject>Depolymerization</subject><subject>Enzymatic activity</subject><subject>Enzyme activity</subject><subject>Enzymes</subject><subject>Extracellular enzymes</subject><subject>Global warming</subject><subject>Glucose</subject><subject>Glucosidase</subject><subject>Heat waves</subject><subject>Heatwaves</subject><subject>Hot summers</subject><subject>Incubation period</subject><subject>Intracellular</subject><subject>Metabolism</subject><subject>Microbial activity</subject><subject>Microorganisms</subject><subject>Mineralization</subject><subject>Moisture content</subject><subject>Molecular weight</subject><subject>Monomers</subject><subject>Observatories</subject><subject>Organic matter</subject><subject>Organic soils</subject><subject>Physiological aspects</subject><subject>Physiological effects</subject><subject>Respiration</subject><subject>Sensitivity</subject><subject>Soil</subject><subject>Soil chemistry</subject><subject>Soil organic matter</subject><subject>Soil pH</subject><subject>Soil temperature</subject><subject>Soil types</subject><subject>Substrates</subject><subject>Temperature</subject><subject>Temperature changes</subject><subject>Temperature effects</subject><subject>β-Glucosidase</subject><issn>1726-4189</issn><issn>1726-4170</issn><issn>1726-4189</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptks2L1TAQwIsouK6evQY8eehuvtqmx2V19cGC4Mc5TJNJyaNtnkkqPv96032i-0BymDD85kdmMlX1mtGrhvXyehhrTmvOaVciF0-qC9bxtpZM9U8f3Z9XL1LaUyoUVc1FFd955zDikj1MJON8wAh5jUgSLsln_8PnIwmO-CVHMDhN6wSRzJhhCJM35BCDwZQwEVgswZ-PqRT8RHD5dZyRgHlweUwvq2cOpoSv_sTL6tvd-6-3H-v7Tx92tzf3tRGyFfXQsAaFapzlqkXXdiBbKoFxZVEqxnrOEbgbjOBNY611BqWxllrjONsMl9Xu5LUB9voQ_QzxqAN4_ZAIcdQQszcTao5OIu1a1RspocUBLBuY6FnbIePN5npzcpV2v6-Yst6HNS7l-Zor3tLyA4r_o0YoUr-4sE1j9snom64RrBcFLdTVf6hyLM7ehAWdL_mzgrdnBYXJZdAjrCnp3ZfP5-z1iTUxpBTR_W2cUb3tiR5Gzane9kRveyJ-A-2RsK4</recordid><startdate>20230616</startdate><enddate>20230616</enddate><creator>Adekanmbi, Adetunji Alex</creator><creator>Dale, Laurence</creator><creator>Shaw, Liz</creator><creator>Sizmur, 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temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities</title><author>Adekanmbi, Adetunji Alex ; Dale, Laurence ; Shaw, Liz ; Sizmur, Tom</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3463-b515e385fd286ef67a4604a128de4811922ea2fbc3255dddfce4cdd0dcf213463</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Acclimatization</topic><topic>Adaptation</topic><topic>Carbon/nitrogen ratio</topic><topic>Chitinase</topic><topic>Climate change</topic><topic>Climate prediction</topic><topic>Decomposition</topic><topic>Depolymerization</topic><topic>Enzymatic activity</topic><topic>Enzyme activity</topic><topic>Enzymes</topic><topic>Extracellular enzymes</topic><topic>Global warming</topic><topic>Glucose</topic><topic>Glucosidase</topic><topic>Heat waves</topic><topic>Heatwaves</topic><topic>Hot summers</topic><topic>Incubation period</topic><topic>Intracellular</topic><topic>Metabolism</topic><topic>Microbial activity</topic><topic>Microorganisms</topic><topic>Mineralization</topic><topic>Moisture content</topic><topic>Molecular weight</topic><topic>Monomers</topic><topic>Observatories</topic><topic>Organic matter</topic><topic>Organic soils</topic><topic>Physiological aspects</topic><topic>Physiological effects</topic><topic>Respiration</topic><topic>Sensitivity</topic><topic>Soil</topic><topic>Soil chemistry</topic><topic>Soil organic matter</topic><topic>Soil pH</topic><topic>Soil temperature</topic><topic>Soil types</topic><topic>Substrates</topic><topic>Temperature</topic><topic>Temperature changes</topic><topic>Temperature effects</topic><topic>β-Glucosidase</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Adekanmbi, Adetunji Alex</creatorcontrib><creatorcontrib>Dale, Laurence</creatorcontrib><creatorcontrib>Shaw, Liz</creatorcontrib><creatorcontrib>Sizmur, 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Journals</collection><jtitle>Biogeosciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Adekanmbi, Adetunji Alex</au><au>Dale, Laurence</au><au>Shaw, Liz</au><au>Sizmur, Tom</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential temperature sensitivity of intracellular metabolic processes and extracellular soil enzyme activities</atitle><jtitle>Biogeosciences</jtitle><date>2023-06-16</date><risdate>2023</risdate><volume>20</volume><issue>11</issue><spage>2207</spage><epage>2219</epage><pages>2207-2219</pages><issn>1726-4189</issn><issn>1726-4170</issn><eissn>1726-4189</eissn><abstract>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
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.</abstract><cop>Katlenburg-Lindau</cop><pub>Copernicus GmbH</pub><doi>10.5194/bg-20-2207-2023</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-9835-7195</orcidid><orcidid>https://orcid.org/0000-0003-3379-4161</orcidid><oa>free_for_read</oa></addata></record> |
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source | Publicly Available Content Database; DOAJ Directory of Open Access Journals |
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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