Microbial diversity drives carbon use efficiency in a model soil
Abstract
Abstract Empirical evidence for the response of soil carbon cycling to the combined effects of warming, drought and diversity loss is scarce. Microbial carbon use efficiency (CUE) plays a central role in regulating the flow of carbon through soil, yet how biotic and abiotic factors interact to drive it remains unclear. Here, we combine distinct community inocula (a biotic factor) with different temperature and moisture conditions (abiotic factors) to manipulate microbial diversity and community structure within a model soil. While community composition and diversity are the strongest predictors of CUE, abiotic factors modulated the relationship between diversity and CUE, with CUE being positively correlated with bacterial diversity only under high moisture. Altogether these results indicate that the diversity × ecosystem-function relationship can be impaired under non-favorable conditions in soils, and that to understand changes in soil C cycling we need to account for the multiple facets of global changes.
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Massachusetts, Amherst, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1642319
- Alternate Identifier(s):
- OSTI ID: 1803059
- Grant/Contract Number:
- SC0016590
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics
Citation Formats
Domeignoz-Horta, Luiz A., Pold, Grace, Liu, Xiao-Jun Allen, Frey, Serita D., Melillo, Jerry M., and DeAngelis, Kristen M. Microbial diversity drives carbon use efficiency in a model soil. United Kingdom: N. p., 2020.
Web. doi:10.1038/s41467-020-17502-z.
Domeignoz-Horta, Luiz A., Pold, Grace, Liu, Xiao-Jun Allen, Frey, Serita D., Melillo, Jerry M., & DeAngelis, Kristen M. Microbial diversity drives carbon use efficiency in a model soil. United Kingdom. https://doi.org/10.1038/s41467-020-17502-z
Domeignoz-Horta, Luiz A., Pold, Grace, Liu, Xiao-Jun Allen, Frey, Serita D., Melillo, Jerry M., and DeAngelis, Kristen M. Thu .
"Microbial diversity drives carbon use efficiency in a model soil". United Kingdom. https://doi.org/10.1038/s41467-020-17502-z.
@article{osti_1642319,
title = {Microbial diversity drives carbon use efficiency in a model soil},
author = {Domeignoz-Horta, Luiz A. and Pold, Grace and Liu, Xiao-Jun Allen and Frey, Serita D. and Melillo, Jerry M. and DeAngelis, Kristen M.},
abstractNote = {Abstract Empirical evidence for the response of soil carbon cycling to the combined effects of warming, drought and diversity loss is scarce. Microbial carbon use efficiency (CUE) plays a central role in regulating the flow of carbon through soil, yet how biotic and abiotic factors interact to drive it remains unclear. Here, we combine distinct community inocula (a biotic factor) with different temperature and moisture conditions (abiotic factors) to manipulate microbial diversity and community structure within a model soil. While community composition and diversity are the strongest predictors of CUE, abiotic factors modulated the relationship between diversity and CUE, with CUE being positively correlated with bacterial diversity only under high moisture. Altogether these results indicate that the diversity × ecosystem-function relationship can be impaired under non-favorable conditions in soils, and that to understand changes in soil C cycling we need to account for the multiple facets of global changes.},
doi = {10.1038/s41467-020-17502-z},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United Kingdom},
year = {Thu Jul 23 00:00:00 EDT 2020},
month = {Thu Jul 23 00:00:00 EDT 2020}
}
https://doi.org/10.1038/s41467-020-17502-z
Web of Science
Works referenced in this record:
An examination of the biodiversity–ecosystem function relationship in arable soil microbial communities
journal, October 2001
- Griffiths, B. S.; Ritz, K.; Wheatley, R.
- Soil Biology and Biochemistry, Vol. 33, Issue 12-13
piecewiseSEM : Piecewise structural equation modelling in r for ecology, evolution, and systematics
journal, December 2015
- Lefcheck, Jonathan S.
- Methods in Ecology and Evolution, Vol. 7, Issue 5
rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development
journal, November 2014
- Stoddard, Steven F.; Smith, Byron J.; Hein, Robert
- Nucleic Acids Research, Vol. 43, Issue D1
Scientists’ warning to humanity: microorganisms and climate change
journal, June 2019
- Cavicchioli, Ricardo; Ripple, William J.; Timmis, Kenneth N.
- Nature Reviews Microbiology, Vol. 17, Issue 9
Peaks of in situ N 2 O emissions are influenced by N 2 O-producing and reducing microbial communities across arable soils
journal, September 2017
- Domeignoz-Horta, Luiz A.; Philippot, Laurent; Peyrard, Celine
- Global Change Biology, Vol. 24, Issue 1
Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA.
journal, January 1993
- Muyzer, G.; de Waal, E. C.; Uitterlinden, A. G.
- Applied and Environmental Microbiology, Vol. 59, Issue 3
Decomposition responses to climate depend on microbial community composition
journal, November 2018
- Glassman, Sydney I.; Weihe, Claudia; Li, Junhui
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 47
Microbial biomass response to a rapid increase in water potential when dry soil is wetted
journal, January 1987
- Kieft, Thomas L.; soroker, Edith; firestone, Mary K.
- Soil Biology and Biochemistry, Vol. 19, Issue 2
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
Soil carbon sensitivity to temperature and carbon use efficiency compared across microbial-ecosystem models of varying complexity
journal, January 2014
- Li, Jianwei; Wang, Gangsheng; Allison, Steven D.
- Biogeochemistry, Vol. 119, Issue 1-3
Mechanisms for soil moisture effects on activity of nitrifying bacteria.
journal, January 1995
- Stark, J. M.; Firestone, M. K.
- Applied and environmental microbiology, Vol. 61, Issue 1
Biodiversity and ecosystem functioning: recent theoretical advances
journal, October 2000
- Loreau, Michel
- Oikos, Vol. 91, Issue 1
Functional diversity revealed by removal experiments
journal, March 2003
- Dı́az, Sandra; Symstad, Amy J.; Stuart Chapin, F.
- Trends in Ecology & Evolution, Vol. 18, Issue 3
Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria
journal, January 2020
- Pold, Grace; Domeignoz-Horta, Luiz A.; Morrison, Eric W.
- mBio, Vol. 11, Issue 1
Soil microbial carbon use efficiency and biomass turnover in a long-term fertilization experiment in a temperate grassland
journal, June 2016
- Spohn, Marie; Pötsch, Erich M.; Eichorst, Stephanie A.
- Soil Biology and Biochemistry, Vol. 97
Changes in temperature alter the relationship between biodiversity and ecosystem functioning
journal, October 2018
- García, Francisca C.; Bestion, Elvire; Warfield, Ruth
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 43
Systematic variation in the temperature dependence of physiological and ecological traits
journal, May 2011
- Dell, A. I.; Pawar, S.; Savage, V. M.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 26
The contribution of species richness and composition to bacterial services
journal, August 2005
- Bell, Thomas; Newman, Jonathan A.; Silverman, Bernard W.
- Nature, Vol. 436, Issue 7054
Environmental and stoichiometric controls on microbial carbon-use efficiency in soils: Research review
journal, July 2012
- Manzoni, Stefano; Taylor, Philip; Richter, Andreas
- New Phytologist, Vol. 196, Issue 1
Genome‐based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles
journal, February 2019
- Lofgren, Lotus A.; Uehling, Jessie K.; Branco, Sara
- Molecular Ecology, Vol. 28, Issue 4
Selective isolation of bioactive soil actinomycetes belonging to the Streptomyces violaceusniger phenotypic cluster
journal, May 2004
- Hayakawa, M.; Yoshida, Y.; Iimura, Y.
- Journal of Applied Microbiology, Vol. 96, Issue 5
Loss in microbial diversity affects nitrogen cycling in soil
journal, March 2013
- Philippot, Laurent; Spor, Aymé; Hénault, Catherine
- The ISME Journal, Vol. 7, Issue 8
Aggregation and Soil Organic Matter Accumulation in Cultivated and Native Grassland Soils
journal, January 1998
- Six, J.; Elliott, E. T.; Paustian, K.
- Soil Science Society of America Journal, Vol. 62, Issue 5
A global synthesis reveals biodiversity loss as a major driver of ecosystem change
journal, May 2012
- Hooper, David U.; Adair, E. Carol; Cardinale, Bradley J.
- Nature, Vol. 486, Issue 7401
Belowground biodiversity and ecosystem functioning
journal, November 2014
- Bardgett, Richard D.; van der Putten, Wim H.
- Nature, Vol. 515, Issue 7528
Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls
journal, November 2016
- Kallenbach, Cynthia M.; Frey, Serita D.; Grandy, A. Stuart
- Nature Communications, Vol. 7, Issue 1
Land use driven change in soil pH affects microbial carbon cycling processes
journal, September 2018
- Malik, Ashish A.; Puissant, Jeremy; Buckeridge, Kate M.
- Nature Communications, Vol. 9, Issue 1
Colorimetric Determination of Oxidizable Carbon in Acid Soil Solutions
journal, January 1988
- Bartlett, Richmond J.; Ross, Donald S.
- Soil Science Society of America Journal, Vol. 52, Issue 4
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world
journal, October 2017
- Melillo, J. M.; Frey, S. D.; DeAngelis, K. M.
- Science, Vol. 358, Issue 6359
The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system
journal, September 2015
- Domeignoz-Horta, Luiz A.; Spor, Aymé; Bru, David
- Frontiers in Microbiology, Vol. 6
Measurement and estimation of the soil water retention curve using the evaporation method and the pseudo continuous pedotransfer function
journal, August 2018
- Haghverdi, Amir; Öztürk, Hasan Sabri; Durner, Wolfgang
- Journal of Hydrology, Vol. 563
Measuring microbial biomass carbon by direct extraction – Comparison with chloroform fumigation-extraction
journal, November 2012
- Setia, Raj; Verma, Suman Lata; Marschner, Petra
- European Journal of Soil Biology, Vol. 53
Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe
journal, August 2015
- Leff, Jonathan W.; Jones, Stuart E.; Prober, Suzanne M.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 35
Examining the fungal and bacterial niche overlap using selective inhibitors in soil: Decomposing fungalâbacterial interaction in soil
journal, March 2008
- Rousk, Johannes; Demoling, Louise Aldén; Bahr, Adam
- FEMS Microbiology Ecology, Vol. 63, Issue 3
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
Soil bacterial networks are less stable under drought than fungal networks
journal, August 2018
- de Vries, Franciska T.; Griffiths, Rob I.; Bailey, Mark
- Nature Communications, Vol. 9, Issue 1
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
Global soil carbon projections are improved by modelling microbial processes
journal, July 2013
- Wieder, William R.; Bonan, Gordon B.; Allison, Steven D.
- Nature Climate Change, Vol. 3, Issue 10
Soil microbial communities with greater investment in resource acquisition have lower growth yield
journal, May 2019
- Malik, Ashish A.; Puissant, Jeremy; Goodall, Tim
- Soil Biology and Biochemistry, Vol. 132
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
Microbial growth efficiencies across a soil moisture gradient assessed using 13C-acetic acid vapor and 15N-ammonia gas
journal, June 2009
- Herron, Patrick M.; Stark, John M.; Holt, Carson
- Soil Biology and Biochemistry, Vol. 41, Issue 6
Increasing aridity reduces soil microbial diversity and abundance in global drylands
journal, December 2015
- Maestre, Fernando T.; Delgado-Baquerizo, Manuel; Jeffries, Thomas C.
- Proceedings of the National Academy of Sciences
Degradation and humification of maize straw in soil microcosms inoculated with simple and complex microbial communities
journal, February 2007
- Liebich, J.; Schloter, M.; Schäffer, A.
- European Journal of Soil Science, Vol. 58, Issue 1
Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity-ecosystem function relationship
journal, August 2000
- Griffiths, B. S.; Ritz, K.; Bardgett, R. D.
- Oikos, Vol. 90, Issue 2
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
journal, July 2019
- Bolyen, Evan; Rideout, Jai Ram; Dillon, Matthew R.
- Nature Biotechnology, Vol. 37, Issue 8
Flow Partitioning in Fully Saturated Soil Aggregates
journal, March 2014
- Yang, Xiaofan; Richmond, Marshall C.; Scheibe, Timothy D.
- Transport in Porous Media, Vol. 103, Issue 2
Reduced carbon use efficiency and increased microbial turnover with soil warming
journal, December 2018
- Li, Jianwei; Wang, Gangsheng; Mayes, Melanie A.
- Global Change Biology
Changes in variability of soil moisture alter microbial community C and N resource use
journal, September 2011
- Tiemann, Lisa K.; Billings, Sharon A.
- Soil Biology and Biochemistry, Vol. 43, Issue 9
Assessment of Soil Microbial Community Structure by Use of Taxon-Specific Quantitative PCR Assays
journal, July 2005
- Fierer, N.; Jackson, J. A.; Vilgalys, R.
- Applied and Environmental Microbiology, Vol. 71, Issue 7
Maintenance of soil functioning following erosion of microbial diversity
journal, December 2006
- Wertz, Sophie; Degrange, Valérie; Prosser, James I.
- Environmental Microbiology, Vol. 8, Issue 12
Microbial growth and carbon use efficiency in soil: Links to fungal-bacterial dominance, SOC-quality and stoichiometry
journal, April 2019
- Soares, Margarida; Rousk, Johannes
- Soil Biology and Biochemistry, Vol. 131
Microbial control over carbon cycling in soil
journal, January 2012
- Schimel, Joshua P.; Schaeffer, Sean M.
- Frontiers in Microbiology, Vol. 3
Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships
journal, November 2010
- Nielsen, U. N.; Ayres, E.; Wall, D. H.
- European Journal of Soil Science, Vol. 62, Issue 1
Metabolic network architecture and carbon source determine metabolite production costs
journal, May 2016
- Waschina, Silvio; D'Souza, Glen; Kost, Christian
- The FEBS Journal, Vol. 283, Issue 11
Soil-carbon response to warming dependent on microbial physiology
journal, April 2010
- Allison, Steven D.; Wallenstein, Matthew D.; Bradford, Mark A.
- Nature Geoscience, Vol. 3, Issue 5
Lack of functional redundancy in the relationship between microbial diversity and ecosystem functioning
journal, May 2016
- Delgado-Baquerizo, Manuel; Giaramida, Luca; Reich, Peter B.
- Journal of Ecology, Vol. 104, Issue 4
Changes in substrate availability drive carbon cycle response to chronic warming
journal, July 2017
- Pold, Grace; Grandy, A. Stuart; Melillo, Jerry M.
- Soil Biology and Biochemistry, Vol. 110
Plant diversity enhances productivity and soil carbon storage
journal, April 2018
- Chen, Shiping; Wang, Wantong; Xu, Wenting
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 16
Cell-to-cell bacterial interactions promoted by drier conditions on soil surfaces
journal, September 2018
- Tecon, Robin; Ebrahimi, Ali; Kleyer, Hannah
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 39
UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi: Methods
journal, March 2005
- Kõljalg, Urmas; Larsson, Karl-Henrik; Abarenkov, Kessy
- New Phytologist, Vol. 166, Issue 3
A New Inferential Test for Path Models Based on Directed Acyclic Graphs
journal, June 2000
- Shipley, Bill
- Structural Equation Modeling: A Multidisciplinary Journal, Vol. 7, Issue 2
The more, the merrier: heterotroph richness stimulates methanotrophic activity
journal, May 2014
- Ho, Adrian; de Roy, Karen; Thas, Olivier
- The ISME Journal, Vol. 8, Issue 9
Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling
journal, April 2013
- Sinsabaugh, Robert L.; Manzoni, Stefano; Moorhead, Daryl L.
- Ecology Letters, Vol. 16, Issue 7
Agriculture's impact on microbial diversity and associated fluxes of carbon dioxide and methane
journal, April 2011
- Levine, Uri Y.; Teal, Tracy K.; Robertson, G. Philip
- The ISME Journal, Vol. 5, Issue 10
Aggregate-Size Stability Distribution and Soil Stability
journal, January 2004
- Márquez, C. O.; Garcia, V. J.; Cambardella, C. A.
- Soil Science Society of America Journal, Vol. 68, Issue 3
Growth explains microbial carbon use efficiency across soils differing in land use and geology
journal, January 2019
- Zheng, Qing; Hu, Yuntao; Zhang, Shasha
- Soil Biology and Biochemistry, Vol. 128
Land-use alters the temperature response of microbial carbon-use efficiency in soils – a consumption-based approach
journal, January 2020
- Bölscher, Tobias; Ågren, Göran I.; Herrmann, Anke M.
- Soil Biology and Biochemistry, Vol. 140
Global patterns in belowground communities
journal, November 2009
- Fierer, Noah; Strickland, Michael S.; Liptzin, Daniel
- Ecology Letters, Vol. 12, Issue 11