Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls

Kallenbach, Cynthia M.; Frey, Serita D.; Grandy, A. Stuart

doi:10.1038/ncomms13630

Title: Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls

Journal Article · Mon Nov 28 00:00:00 EST 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms13630· OSTI ID:1363941

Kallenbach, Cynthia M. ^[1]; Frey, Serita D. ^[2]; Grandy, A. Stuart ^[2]

Univ. of New Hampshire, Durham, NH (United States); Colorado State Univ., Fort Collins, CO (United States)
Univ. of New Hampshire, Durham, NH (United States)

Soil organic matter (SOM) and the carbon and nutrients therein drive fundamental submicron- to global-scale biogeochemical processes and influence carbon-climate feedbacks. Consensus is emerging that microbial materials are an important constituent of stable SOM, and new conceptual and quantitative SOM models are rapidly incorporating this view. However, direct evidence demonstrating that microbial residues account for the chemistry, stability and abundance of SOM is still lacking. Further, emerging models emphasize the stabilization of microbial-derived SOM by abiotic mechanisms, while the effects of microbial physiology on microbial residue production remain unclear. Here we provide the first direct evidence that soil microbes produce chemically diverse, stable SOM. As a result, we show that SOM accumulation is driven by distinct microbial communities more so than clay mineralogy, where microbial-derived SOM accumulation is greatest in soils with higher fungal abundances and more efficient microbial biomass production.

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Research Organization:: Univ. of New Hampshire, Durham, NH (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1363941

Journal Information:: Nature Communications, Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 795 works

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Examining mineral-associated soil organic matter pools through depth in harvested forest soil profiles Gabriel, C. E.; Kellman, L.; Prest, D. PLOS ONE, Vol. 13, Issue 11 https://doi.org/10.1371/journal.pone.0206847	journal	November 2018
Lignin Contribution to Aliphatic Constituents of Humic Acids through Fungal Degradation Khatami, Seyyedhadi; Deng, Ying; Tien, Ming Journal of Environmental Quality, Vol. 48, Issue 6 https://doi.org/10.2134/jeq2019.01.0034	journal	November 2019
Translocation of Carbon from Surface Organic Horizons to the Subsoil in Coarse-Textured Spodosols: Implications for Deep Soil C Dynamics Rothstein, David E.; Toosi, Ehsan R.; Schaetzl, Randall J. Soil Science Society of America Journal, Vol. 82, Issue 4 https://doi.org/10.2136/sssaj2018.01.0033	journal	July 2018
Influence of Groundcover Vegetation, Soil Physicochemical Properties, and Irrigation Practices on Soil Fungi in Semi-arid Vineyards Vukicevich, Eric; Lowery, D. Thomas; Bennett, Jonathan A. Frontiers in Ecology and Evolution, Vol. 7 https://doi.org/10.3389/fevo.2019.00118	journal	April 2019
Constraining Carbon and Nutrient Flows in Soil With Ecological Stoichiometry Buchkowski, Robert W.; Shaw, Alanna N.; Sihi, Debjani Frontiers in Ecology and Evolution, Vol. 7 https://doi.org/10.3389/fevo.2019.00382	journal	October 2019
Soil Biological Fertility and Bacterial Community Response to Land Use Intensity: A Case Study in the Mediterranean Area Yaghoubi Khanghahi, Mohammad; Murgese, Pasqua; Strafella, Sabrina Diversity, Vol. 11, Issue 11 https://doi.org/10.3390/d11110211	journal	November 2019
A Molecular Investigation of Soil Organic Carbon Composition across a Subalpine Catchment Hsu, Hsiao-Tieh; Lawrence, Corey; Winnick, Matthew Soil Systems, Vol. 2, Issue 1 https://doi.org/10.3390/soils2010006	journal	February 2018
Biotic versus Abiotic Controls on Bioavailable Soil Organic Carbon Blankinship, Joseph; Schimel, Joshua Soil Systems, Vol. 2, Issue 1 https://doi.org/10.3390/soilsystems2010010	journal	February 2018
Applying Soil Health Indicators to Encourage Sustainable Soil Use: The Transition from Scientific Study to Practical Application Griffiths, Bryan; Faber, Jack; Bloem, Jaap Sustainability, Vol. 10, Issue 9 https://doi.org/10.3390/su10093021	journal	August 2018
Reviews and syntheses: Carbon use efficiency from organisms to ecosystems – definitions, theories, and empirical evidence Manzoni, Stefano; Čapek, Petr; Porada, Philipp Biogeosciences, Vol. 15, Issue 19 https://doi.org/10.5194/bg-15-5929-2018	journal	January 2018
Metabolic tradeoffs and heterogeneity in microbial responses to temperature determine the fate of litter carbon in simulations of a warmer world Pold, Grace; Sistla, Seeta A.; DeAngelis, Kristen M. Biogeosciences, Vol. 16, Issue 24 https://doi.org/10.5194/bg-16-4875-2019	journal	January 2019
Environmental filtering drives bacterial community structure and function in a subalpine area of northern China Zhao, Pengyu; Liu, Jinxian; Jia, Tong Journal of Basic Microbiology, Vol. 59, Issue 3 https://doi.org/10.1002/jobm.201800314	journal	December 2018
Enhanced microbial respiration due to carbon sequestration in pruning litter incorporated soil reduced the net carbon dioxide flux from atmosphere to tea ecosystem Pramanik, Prabhat; Phukan, Manabjyoti Journal of the Science of Food and Agriculture, Vol. 100, Issue 1 https://doi.org/10.1002/jsfa.10038	journal	October 2019
Lasting effects of soil health improvements with management changes in cotton-based cropping systems in a sandy soil Acosta-Martínez, V.; Cotton, J. Biology and Fertility of Soils, Vol. 53, Issue 5 https://doi.org/10.1007/s00374-017-1192-2	journal	May 2017
Litter quantity, litter chemistry, and soil texture control changes in soil organic carbon fractions under bioenergy cropping systems of the North Central U.S. von Haden, Adam C.; Kucharik, Christopher J.; Jackson, Randall D. Biogeochemistry, Vol. 143, Issue 3 https://doi.org/10.1007/s10533-019-00564-7	journal	April 2019
Concentration-dependent responses of soil bacterial, fungal and nitrifying communities to silver nano and micron particles McGee, Conor Francis; Storey, Sean; Clipson, Nicholas Environmental Science and Pollution Research, Vol. 25, Issue 19 https://doi.org/10.1007/s11356-018-2087-y	journal	April 2018
Stoichiometry constraints challenge the potential of agroecological practices for the soil C storage. A review Bertrand, Isabelle; Viaud, Valérie; Daufresne, Tanguy Agronomy for Sustainable Development, Vol. 39, Issue 6 https://doi.org/10.1007/s13593-019-0599-6	journal	November 2019
Land use driven change in soil pH affects microbial carbon cycling processes Malik, Ashish A.; Puissant, Jeremy; Buckeridge, Kate M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05980-1	journal	September 2018
Plant roots increase both decomposition and stable organic matter formation in boreal forest soil Adamczyk, Bartosz; Sietiö, Outi-Maaria; Straková, Petra Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11993-1	journal	September 2019
Climate-smart crops with enhanced photosynthesis Jansson, Christer; Vogel, John; Hazen, Samuel Journal of Experimental Botany, Vol. 69, Issue 16 https://doi.org/10.1093/jxb/ery213	journal	May 2018
Crop traits drive soil carbon sequestration under organic farming García-Palacios, Pablo; Gattinger, Andreas; Bracht-Jørgensen, Helene Journal of Applied Ecology, Vol. 55, Issue 5 https://doi.org/10.1111/1365-2664.13113	journal	February 2018
Microbial community assembly differs across minerals in a rhizosphere microcosm Whitman, Thea; Neurath, Rachel; Perera, Adele Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14366	journal	September 2018
Carbon cycle confidence and uncertainty: Exploring variation among soil biogeochemical models Wieder, William R.; Hartman, Melannie D.; Sulman, Benjamin N. Global Change Biology, Vol. 24, Issue 4 https://doi.org/10.1111/gcb.13979	journal	November 2017
Organic carbon stocks in the Russian Chernozem: Carbon stocks of Chernozems Mikhailova, E. A.; Post, C. J. European Journal of Soil Science, Vol. 57, Issue 3 https://doi.org/10.1111/j.1365-2389.2005.00741.x	journal	June 2005
Impact of silver nanoparticles (AgNP) on soil microbial community depending on functionalization, concentration, exposure time, and soil texture Grün, Anna-Lena; Manz, Werner; Kohl, Yvonne Lydia Environmental Sciences Europe, Vol. 31, Issue 1 https://doi.org/10.1186/s12302-019-0196-y	journal	February 2019
Grazing-induced microbiome alterations drive soil organic carbon turnover and productivity in meadow steppe Xun, Weibing; Yan, Ruirui; Ren, Yi Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0544-y	journal	September 2018
Nitrogen fertilization modifies organic transformations and coatings on soil biogeochemical interfaces through microbial polysaccharides synthesis Huang, Xizhi; Guggenberger, Georg; Kuzyakov, Yakov London : Nature Publishing Group https://doi.org/10.15488/10501	other	January 2019
Microaggregates in soils Totsche, Kai Uwe; Amelung, Wulf; Gerzabek, Martin H. Weinheim : Wiley-VCH Verlag https://doi.org/10.15488/3363	other	January 2018
Carbon Amendments Induce Shifts in Nutrient Use, Inhibitory, and Resistance Phenotypes Among Soilborne Streptomyces Dundore-Arias, José Pablo; Felice, Laura; Dill-Macky, Ruth Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00498	journal	March 2019
Composition-Dependent Sorptive Fractionation of Anthropogenic Dissolved Organic Matter by Fe(III)-Montmorillonite Young, Robert; Avneri-Katz, Shani; McKenna, Amy Soil Systems, Vol. 2, Issue 1 https://doi.org/10.3390/soilsystems2010014	journal	March 2018
What Agriculture Can Learn from Native Ecosystems in Building Soil Organic Matter: A Review Crews, Timothy; Rumsey, Brian Sustainability, Vol. 9, Issue 4 https://doi.org/10.3390/su9040578	journal	April 2017
Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity Prommer, Judith; Walker, Tom W. N.; Wanek, Wolfgang ETH Zurich https://doi.org/10.3929/ethz-b-000365575	text	January 2020
Constraining carbon and nutrient flows in soil with ecological stoichiometry Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani Zenodo https://doi.org/10.5281/zenodo.3464584	text	January 2019
Multiple models and experiments underscore large uncertainty in soil carbon dynamics Sulman, Benjamin N.; Moore, Jessica A. M.; Abramoff, Rose Biogeochemistry, Vol. 141, Issue 2 https://doi.org/10.1007/s10533-018-0509-z	journal	October 2018
Sub-micron level investigation reveals the inaccessibility of stabilized carbon in soil microaggregates Arachchige, Pavithra S. Pitumpe; Hettiarachchi, Ganga M.; Rice, Charles W. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34981-9	journal	November 2018
Dark microbial CO ₂ fixation in temperate forest soils increases with CO ₂ concentration Spohn, Marie; Müller, Karolin; Höschen, Carmen Global Change Biology, Vol. 26, Issue 3 https://doi.org/10.1111/gcb.14937	journal	December 2019
Nitrogen fertilization modifies organic transformations and coatings on soil biogeochemical interfaces through microbial polysaccharides synthesis Huang, Xizhi; Guggenberger, Georg; Kuzyakov, Yakov London : Nature Publishing Group https://doi.org/10.15488/10477	other	January 2019
Microbial and abiotic controls on mineral-associated organic matter in soil profiles along an ecosystem gradient Mikutta, Robert; Turner, Stephanie; Schippers, Axel Berlin : Springer https://doi.org/10.15488/8622	other	January 2019
The Millennial model: in search of measurable pools and transformations for modeling soil carbon in the new century Abramoff, Rose; Xu, Xiaofeng; Hartman, Melannie Biogeochemistry, Vol. 137, Issue 1-2 https://doi.org/10.1007/s10533-017-0409-7	journal	December 2017
Networking our science to characterize the state, vulnerabilities, and management opportunities of soil organic matter Harden, Jennifer W.; Hugelius, Gustaf; Ahlström, Anders Global Change Biology, Vol. 24, Issue 2 https://doi.org/10.1111/gcb.13896	journal	September 2017
Tree mycorrhizal type predicts within-site variability in the storage and distribution of soil organic matter Craig, Matthew E.; Turner, Benjamin L.; Liang, Chao Global Change Biology, Vol. 24, Issue 8 https://doi.org/10.1111/gcb.14132	journal	April 2018
Niche differentiation is spatially and temporally regulated in the rhizosphere Nuccio, Erin E.; Starr, Evan; Karaoz, Ulas The ISME Journal, Vol. 14, Issue 4 https://doi.org/10.1038/s41396-019-0582-x	journal	January 2020
Microbial community-level regulation explains soil carbon responses to long-term litter manipulations Georgiou, Katerina; Abramoff, Rose Z.; Harte, John Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01116-z	journal	October 2017
Online supercritical fluid extraction mass spectrometry (SFE-LC-FTMS) for sensitive characterization of soil organic matter Shen, Yufeng; Zhao, Rui; Tolić, Nikola Faraday Discussions, Vol. 218 https://doi.org/10.1039/c9fd00011a	journal	January 2019
Constraining carbon and nutrient flows in soil with ecological stoichiometry Buchkowski, Robert; Shaw, Alanna; Sihi, Debjani Zenodo https://doi.org/10.5281/zenodo.3464585	text	January 2019
Tamm Review: Influence of forest management activities on soil organic carbon stocks: A knowledge synthesis Mayer, Mathias; Prescott, Cindy E.; Abaker, Wafa E. A. Forest Ecology and Management, Vol. 466 https://doi.org/10.1016/j.foreco.2020.118127	journal	June 2020
Persistence of soil organic carbon caused by functional complexity Lehmann, Johannes; Hansel, Colleen M.; Kaiser, Christina Nature Geoscience, Vol. 13, Issue 8 https://doi.org/10.1038/s41561-020-0612-3	journal	July 2020
Long-term Management Effects and Temperature Sensitivity of Soil Organic Carbon in Grassland and Agricultural Soils Ghimire, Rajan; Bista, Prakriti; Machado, Stephen Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-48237-7	journal	August 2019
Soil microbiome transfer method affects microbiome composition, including dominant microorganisms, in a novel environment Howard, Mia M.; Bell, Terrence H.; Kao-Kniffin, Jenny FEMS Microbiology Letters, Vol. 364, Issue 11 https://doi.org/10.1093/femsle/fnx092	journal	May 2017
Control of the Nitrogen Isotope Composition of the Fungal Biomass: Evidence of Microbial Nitrogen Use Efficiency Shinoda, Kazuki; Yano, Midori; Yoh, Muneoki Microbes and Environments, Vol. 34, Issue 1 https://doi.org/10.1264/jsme2.me18082	journal	January 2019
Resource Legacies of Organic and Conventional Management Differentiate Soil Microbial Carbon Use Arcand, Melissa M.; Levy-Booth, David J.; Helgason, Bobbi L. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02293	journal	November 2017
Managing Agroecosystems for Soil Microbial Carbon Use Efficiency: Ecological Unknowns, Potential Outcomes, and a Path Forward Kallenbach, Cynthia M.; Wallenstein, Matthew D.; Schipanksi, Meagan E. Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01146	journal	May 2019
Variation in the Molecular Structure and Radiocarbon Abundance of Mineral-Associated Organic Matter across a Lithosequence of Forest Soils Heckman, Katherine; Throckmorton, Heather; Horwath, William Soil Systems, Vol. 2, Issue 2 https://doi.org/10.3390/soilsystems2020036	journal	June 2018
Cover Crop Residue Amount and Quality Effects on Soil Organic Carbon Mineralization Ghimire, Binod; Ghimire, Rajan; VanLeeuwen, Dawn Sustainability, Vol. 9, Issue 12 https://doi.org/10.3390/su9122316	journal	December 2017

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