Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

ABSTRACT The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized t...

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Autores principales:	Grace Pold, Luiz A. Domeignoz-Horta, Eric W. Morrison, Serita D. Frey, Seeta A. Sistla, Kristen M. DeAngelis
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	carbon use efficiency comparative genomics growth strategy physiology soil bacteria Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/1d56777a03c849609174120a63a86d19
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spelling	oai:doaj.org-article:1d56777a03c849609174120a63a86d192021-11-15T15:56:58ZCarbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria10.1128/mBio.02293-192150-7511https://doaj.org/article/1d56777a03c849609174120a63a86d192020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02293-19https://doaj.org/toc/2150-7511ABSTRACT The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought. IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.Grace PoldLuiz A. Domeignoz-HortaEric W. MorrisonSerita D. FreySeeta A. SistlaKristen M. DeAngelisAmerican Society for Microbiologyarticlecarbon use efficiencycomparative genomicsgrowth strategyphysiologysoil bacteriaMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbon use efficiency comparative genomics growth strategy physiology soil bacteria Microbiology QR1-502
spellingShingle	carbon use efficiency comparative genomics growth strategy physiology soil bacteria Microbiology QR1-502 Grace Pold Luiz A. Domeignoz-Horta Eric W. Morrison Serita D. Frey Seeta A. Sistla Kristen M. DeAngelis Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
description	ABSTRACT The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought. IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.
format	article
author	Grace Pold Luiz A. Domeignoz-Horta Eric W. Morrison Serita D. Frey Seeta A. Sistla Kristen M. DeAngelis
author_facet	Grace Pold Luiz A. Domeignoz-Horta Eric W. Morrison Serita D. Frey Seeta A. Sistla Kristen M. DeAngelis
author_sort	Grace Pold
title	Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
title_short	Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
title_full	Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
title_fullStr	Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
title_full_unstemmed	Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
title_sort	carbon use efficiency and its temperature sensitivity covary in soil bacteria
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/1d56777a03c849609174120a63a86d19
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Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

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