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Title: Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Journal Article · · mBio (Online)

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. 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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Univ. of Massachusetts, Amherst, MA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231; SC0016590
OSTI ID:
1592502
Alternate ID(s):
OSTI ID: 1626147
Journal Information:
mBio (Online), Vol. 11, Issue 1; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 39 works
Citation information provided by
Web of Science

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Arthrobacter alpinus sp. nov., a psychrophilic bacterium isolated from alpine soil journal October 2009
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Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits are more Labile journal April 2003
Evidence for a temperature acclimation mechanism in bacteria: an empirical test of a membrane-mediated trade-off: Temperature acclimation in bacteria journal April 2010
Environmental and stoichiometric controls on microbial carbon-use efficiency in soils: Research review journal July 2012
Cooperation and Competition in the Evolution of ATP-Producing Pathways journal April 2001
Soil Warming and Carbon-Cycle Feedbacks to the Climate System journal December 2002
A global atlas of the dominant bacteria found in soil journal January 2018
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IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences journal August 2018
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Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses journal January 2013
Variations of Box Plots journal February 1978
Differential Growth Responses of Soil Bacterial Taxa to Carbon Substrates of Varying Chemical Recalcitrance journal January 2011
Extracellular enzyme production and cheating in Pseudomonas fluorescens depend on diffusion rates journal April 2014
Modeling adaptation of carbon use efficiency in microbial communities journal October 2014
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Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem journal January 2016
Drivers of Bacterial Maintenance and Minimal Energy Requirements journal January 2017
Repeated Measures Correlation journal April 2017
Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model journal January 2014

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