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

Abstract

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.more » 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.« less


Citation Formats

Pold, Grace, Domeignoz-Horta, Luiz A., Morrison, Eric W., Frey, Serita D., Sistla, Seeta A., DeAngelis, Kristen M., and Giovannoni, ed., Stephen J. Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria. United States: N. p., 2020. Web. doi:10.1128/mBio.02293-19.
Pold, Grace, Domeignoz-Horta, Luiz A., Morrison, Eric W., Frey, Serita D., Sistla, Seeta A., DeAngelis, Kristen M., & Giovannoni, ed., Stephen J. Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria. United States. doi:10.1128/mBio.02293-19.
Pold, Grace, Domeignoz-Horta, Luiz A., Morrison, Eric W., Frey, Serita D., Sistla, Seeta A., DeAngelis, Kristen M., and Giovannoni, ed., Stephen J. Tue . "Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria". United States. doi:10.1128/mBio.02293-19.
@article{osti_1592502,
title = {Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria},
author = {Pold, Grace and Domeignoz-Horta, Luiz A. and Morrison, Eric W. and Frey, Serita D. and Sistla, Seeta A. and DeAngelis, Kristen M. and Giovannoni, ed., Stephen J.},
abstractNote = {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.},
doi = {10.1128/mBio.02293-19},
journal = {mBio (Online)},
number = 1,
volume = 11,
place = {United States},
year = {2020},
month = {1}
}

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DOI: 10.1128/mBio.02293-19

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Works referenced in this record:

Drivers of Bacterial Maintenance and Minimal Energy Requirements
journal, January 2017

  • Kempes, Christopher P.; van Bodegom, Peter M.; Wolpert, David
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.00031

Phylogeny of Bacterial and Archaeal Genomes Using Conserved Genes: Supertrees and Supermatrices
journal, April 2013


Availability of public goods shapes the evolution of competing metabolic strategies
journal, August 2013

  • Bachmann, H.; Fischlechner, M.; Rabbers, I.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 35
  • DOI: 10.1073/pnas.1308523110

Microbial temperature sensitivity and biomass change explain soil carbon loss with warming
journal, September 2018

  • Walker, Tom W. N.; Kaiser, Christina; Strasser, Florian
  • Nature Climate Change, Vol. 8, Issue 10
  • DOI: 10.1038/s41558-018-0259-x

Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins
journal, August 2010


Arthrobacter alpinus sp. nov., a psychrophilic bacterium isolated from alpine soil
journal, October 2009

  • Zhang, D. -C.; Schumann, P.; Liu, H. -C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 60, Issue 9
  • DOI: 10.1099/ijs.0.017178-0

Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006

  • DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
  • DOI: 10.1128/AEM.03006-05

Enhanced root exudation stimulates soil nitrogen transformations in a subalpine coniferous forest under experimental warming
journal, April 2013

  • Yin, Huajun; Li, Yufei; Xiao, Juan
  • Global Change Biology, Vol. 19, Issue 7
  • DOI: 10.1111/gcb.12161

Fungal Taxa Target Different Carbon Sources in Forest Soil
journal, September 2008


Loss of Genetic Redundancy in Reductive Genome Evolution
journal, February 2011

  • Mendonça, André G.; Alves, Renato J.; Pereira-Leal, José B.
  • PLoS Computational Biology, Vol. 7, Issue 2
  • DOI: 10.1371/journal.pcbi.1001082

Laboratory evolution reveals a two-dimensional rate-yield tradeoff in microbial metabolism
journal, June 2019


Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
journal, August 2013

  • Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
  • Nature Biotechnology, Vol. 31, Issue 9
  • DOI: 10.1038/nbt.2676

Life History Implications of rRNA Gene Copy Number in Escherichia coli
journal, November 2004


Complete genome sequence of Chitinophaga pinensis type strain (UQM 2034T)
journal, February 2010

  • Glavina Del Rio, Tijana; Abt, Birte; Spring, Stefan
  • Standards in Genomic Sciences, Vol. 2, Issue 1
  • DOI: 10.4056/sigs.661199

Microbial response to simulated global change is phylogenetically conserved and linked with functional potential
journal, June 2015

  • Amend, Anthony S.; Martiny, Adam C.; Allison, Steven D.
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.96

New Strategies for Cultivation and Detection of Previously Uncultured Microbes
journal, August 2004


phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package
journal, December 2011


Biotic interactions mediate soil microbial feedbacks to climate change
journal, May 2015

  • Crowther, Thomas W.; Thomas, Stephen M.; Maynard, Daniel S.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 22
  • DOI: 10.1073/pnas.1502956112

Environmental and stoichiometric controls on microbial carbon-use efficiency in soils: Research review
journal, July 2012


Maintenance energy: a general model for energy-limited and energy-sufficient growth
journal, January 1982


SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011

  • Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
  • Nature Methods, Vol. 8, Issue 10
  • DOI: 10.1038/nmeth.1701

Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally
journal, July 2019

  • Ye, Jian‐Sheng; Bradford, Mark A.; Dacal, Marina
  • Global Change Biology, Vol. 25, Issue 10
  • DOI: 10.1111/gcb.14738

BioV Suite - a collection of programs for the study of transport protein evolution: The BioV Suite
journal, May 2012


Draft Genome Sequences of Three Strains of a Novel Rhizobiales Species Isolated from Forest Soil
journal, February 2018


Comparison of temperature effects on soil respiration and bacterial and fungal growth rates
journal, March 2005

  • PietikÃ¥inen, Janna; Pettersson, Marie; Bååth, Erland
  • FEMS Microbiology Ecology, Vol. 52, Issue 1
  • DOI: 10.1016/j.femsec.2004.10.002

Glycolytic strategy as a tradeoff between energy yield and protein cost
journal, April 2013

  • Flamholz, A.; Noor, E.; Bar-Even, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 24
  • DOI: 10.1073/pnas.1215283110

Use of Adaptive Laboratory Evolution To Discover Key Mutations Enabling Rapid Growth of Escherichia coli K-12 MG1655 on Glucose Minimal Medium
journal, October 2014

  • LaCroix, Ryan A.; Sandberg, Troy E.; O'Brien, Edward J.
  • Applied and Environmental Microbiology, Vol. 81, Issue 1
  • DOI: 10.1128/AEM.02246-14

Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

GEIGER: investigating evolutionary radiations
journal, November 2007


The Systemic Imprint of Growth and Its Uses in Ecological (Meta)Genomics
journal, January 2010


Transfer of Pimelobacter tumescens to Terrabacter gen. nov. as Terrabacter tumescens comb. nov. and of Pimelobacter jensenii to Nocardioides as Nocardioides jensenii comb. nov.
journal, January 1989

  • Collins, M. D.; Dorsch, M.; Stackebrandt, E.
  • International Journal of Systematic Bacteriology, Vol. 39, Issue 1
  • DOI: 10.1099/00207713-39-1-1

Inferring the historical patterns of biological evolution
journal, October 1999


The Crabtree Effect: A Regulatory System in Yeast
journal, August 1966


TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life
journal, November 2016

  • Elbourne, Liam D. H.; Tetu, Sasha G.; Hassan, Karl A.
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1068

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Variations of Box Plots
journal, February 1978


Cooperation and Competition in the Evolution of ATP-Producing Pathways
journal, April 2001


A communal catalogue reveals Earth’s multiscale microbial diversity
journal, November 2017

  • Thompson, Luke R.; Sanders, Jon G.; McDonald, Daniel
  • Nature, Vol. 551, Issue 7681
  • DOI: 10.1038/nature24621

Genome Sequence of Verrucomicrobium sp. Strain GAS474, a Novel Bacterium Isolated from Soil
journal, January 2018


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Exploiting rRNA operon copy number to investigate bacterial reproductive strategies
journal, September 2016

  • Roller, Benjamin R. K.; Stoddard, Steven F.; Schmidt, Thomas M.
  • Nature Microbiology, Vol. 1, Issue 11
  • DOI: 10.1038/nmicrobiol.2016.160

Root standing crop and chemistry after six years of soil warming in a temperate forest
journal, July 2011


Soil microbial communities with greater investment in resource acquisition have lower growth yield
journal, May 2019


The temperature response of soil microbial efficiency and its feedback to climate
journal, January 2013

  • Frey, Serita D.; Lee, Juhwan; Melillo, Jerry M.
  • Nature Climate Change, Vol. 3, Issue 4
  • DOI: 10.1038/nclimate1796

The effect of temperature and substrate quality on the carbon use efficiency of saprotrophic decomposition
journal, November 2016


MAPLE 2.3.0: an improved system for evaluating the functionomes of genomes and metagenomes
journal, May 2018

  • Arai, Wataru; Taniguchi, Takeaki; Goto, Susumu
  • Bioscience, Biotechnology, and Biochemistry, Vol. 82, Issue 9
  • DOI: 10.1080/09168451.2018.1476122

The Transporter Classification Database (TCDB): recent advances
journal, November 2015

  • Saier, Milton H.; Reddy, Vamsee S.; Tsu, Brian V.
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1103

Accelerated microbial turnover but constant growth efficiency with warming in soil
journal, September 2014

  • Hagerty, Shannon B.; van Groenigen, Kees Jan; Allison, Steven D.
  • Nature Climate Change, Vol. 4, Issue 10
  • DOI: 10.1038/nclimate2361

Microbial Maintenance: A Critical Review on Its Quantification
journal, March 2007


Repeated Measures Correlation
journal, April 2017


Modeling adaptation of carbon use efficiency in microbial communities
journal, October 2014


The bacterial species definition in the genomic era
journal, October 2006

  • Konstantinidis, Konstantinos T.; Ramette, Alban; Tiedje, James M.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1475
  • DOI: 10.1098/rstb.2006.1920

Integrating microbial physiology and physio-chemical principles in soils with the MIcrobial-MIneral Carbon Stabilization (MIMICS) model
journal, January 2014


Microbial carbon use efficiency and biomass turnover times depending on soil depth – Implications for carbon cycling
journal, May 2016


Predicting microbial traits with phylogenies
journal, September 2015


Reduced carbon use efficiency and increased microbial turnover with soil warming
journal, December 2018

  • Li, Jianwei; Wang, Gangsheng; Mayes, Melanie A.
  • Global Change Biology
  • DOI: 10.1111/gcb.14517

Performance of the Translational Apparatus Varies with the Ecological Strategies of Bacteria
journal, February 2007

  • Dethlefsen, L.; Schmidt, T. M.
  • Journal of Bacteriology, Vol. 189, Issue 8
  • DOI: 10.1128/JB.01686-06

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Long-term forest soil warming alters microbial communities in temperate forest soils
journal, February 2015

  • DeAngelis, Kristen M.; Pold, Grace; TopçuoÄŸlu, Begüm D.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.00104

Evidence for a temperature acclimation mechanism in bacteria: an empirical test of a membrane-mediated trade-off: Temperature acclimation in bacteria
journal, April 2010


Soil Warming and Carbon-Cycle Feedbacks to the Climate System
journal, December 2002


Differential Growth Responses of Soil Bacterial Taxa to Carbon Substrates of Varying Chemical Recalcitrance
journal, January 2011

  • Goldfarb, Katherine C.; Karaoz, Ulas; Hanson, China A.
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00094

Incorporating 16S Gene Copy Number Information Improves Estimates of Microbial Diversity and Abundance
journal, October 2012


Development of microbial-enzyme-mediated decomposition model parameters through steady-state and dynamic analyses
journal, January 2013

  • Wang, Gangsheng; Post, Wilfred M.; Mayes, Melanie A.
  • Ecological Applications, Vol. 23, Issue 1
  • DOI: 10.1890/12-0681.1

Metabolic costs of amino acid and protein production in Escherichia coli
journal, July 2013

  • Kaleta, Christoph; Schäuble, Sascha; Rinas, Ursula
  • Biotechnology Journal, Vol. 8, Issue 9
  • DOI: 10.1002/biot.201200267

dbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation
journal, October 2017

  • Huang, Le; Zhang, Han; Wu, Peizhi
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx894

Probing carbon flux patterns through soil microbial metabolic networks using parallel position-specific tracer labeling
journal, January 2011


Changes in substrate availability drive carbon cycle response to chronic warming
journal, July 2017


Biochemical limits to microbial growth yields: An analysis of mixed substrate utilization
journal, June 1988

  • Gommers, P. J. F.; van Schie, B. J.; van Dijken, J. P.
  • Biotechnology and Bioengineering, Vol. 32, Issue 1
  • DOI: 10.1002/bit.260320112

IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes
journal, October 2018

  • Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky901

The influence of microbial communities, management, and soil texture on soil organic matter chemistry
journal, May 2009


A global atlas of the dominant bacteria found in soil
journal, January 2018

  • Delgado-Baquerizo, Manuel; Oliverio, Angela M.; Brewer, Tess E.
  • Science, Vol. 359, Issue 6373
  • DOI: 10.1126/science.aap9516

IDTAXA: a novel approach for accurate taxonomic classification of microbiome sequences
journal, August 2018


Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem
journal, January 2016

  • Valdivia-Anistro, Jorge A.; Eguiarte-Fruns, Luis E.; Delgado-Sapién, Gabriela
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01486

Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils
journal, September 2016

  • Pold, Grace; Billings, Andrew F.; Blanchard, Jeff L.
  • Applied and Environmental Microbiology, Vol. 82, Issue 22
  • DOI: 10.1128/AEM.02012-16

Life under extreme energy limitation: a synthesis of laboratory- and field-based investigations
journal, May 2015

  • Lever, Mark A.; Rogers, Karyn L.; Lloyd, Karen G.
  • FEMS Microbiology Reviews, Vol. 39, Issue 5
  • DOI: 10.1093/femsre/fuv020

Extracellular enzyme production and cheating in Pseudomonas fluorescens depend on diffusion rates
journal, April 2014


Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits are more Labile
journal, April 2003


Picante: R tools for integrating phylogenies and ecology
journal, April 2010


Community structure follows simple assembly rules in microbial microcosms
journal, March 2017

  • Friedman, Jonathan; Higgins, Logan M.; Gore, Jeff
  • Nature Ecology & Evolution, Vol. 1, Issue 5
  • DOI: 10.1038/s41559-017-0109

Growth explains microbial carbon use efficiency across soils differing in land use and geology
journal, January 2019


Toward an Ecological Classification of soil Bacteria
journal, June 2007

  • Fierer, Noah; Bradford, Mark A.; Jackson, Robert B.
  • Ecology, Vol. 88, Issue 6
  • DOI: 10.1890/05-1839