Molecular Insights into Arctic Soil Organic Matter Degradation under Warming

Chen, Hongmei; Yang, Ziming; Chu, Rosalie K.; Tolic, Nikola; Liang, Liyuan; Graham, David E.; Wullschleger, Stan D.; Gu, Baohua

doi:10.1021/acs.est.7b05469

Title: Molecular Insights into Arctic Soil Organic Matter Degradation under Warming

Journal Article · Fri Mar 23 00:00:00 EDT 2018 · Environmental Science and Technology

DOI:https://doi.org/10.1021/acs.est.7b05469· OSTI ID:1433414

^[1];

^[2]; Chu, Rosalie K. ^[3];

^[3]; Liang, Liyuan ^[3];

^[4]; Wullschleger, Stan D. ^[1];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Oakland Univ., Rochester, MI (United States). Dept. of Chemistry
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division

Molecular composition of the Arctic soil organic carbon (SOC) and its susceptibility to microbial degradation are uncertain due to heterogeneity and unknown SOC compositions. Using ultrahigh-resolution mass spectrometry, we determined the susceptibility and compositional changes of extractable dissolved organic matter (EDOM) in an anoxic warming incubation experiment (up to 122 days) with a tundra soil from Alaska (United States). EDOM was extracted with 10 mM NH4HCO3 from both the organic- and mineral-layer soils during incubation at both -2 and 8 °C. Based on their O:C and H:C ratios, EDOM molecular formulas were qualitatively grouped into nine biochemical classes of compounds, among which lignin-like compounds dominated both the organic and the mineral soils and were the most stable, whereas amino sugars, peptides, and carbohydrate-like compounds were the most biologically labile. These results corresponded with shifts in EDOM elemental composition in which the ratios of O:C and N:C decreased, while the average C content in EDOM, molecular mass, and aromaticity increased after 122 days of incubation. This research demonstrates that certain EDOM components, such as amino sugars, peptides, and carbohydrate-like compounds, are disproportionately more susceptible to microbial degradation than others in the soil, and these results should be considered in SOC degradation models to improve predictions of Arctic climate feedbacks.

View Journal Article

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1433414

Alternate ID(s):: OSTI ID: 1437889; OSTI ID: 1508778

Journal Information:: Environmental Science and Technology, Journal Name: Environmental Science and Technology Vol. 52 Journal Issue: 8; ISSN 0013-936X

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 58 works

Citation information provided by
Web of Science

References (54)

Permafrost carbon−climate feedback is sensitive to deep soil carbon decomposability but not deep soil nitrogen dynamics Koven, Charles D.; Lawrence, David M.; Riley, William J. Proceedings of the National Academy of Sciences https://doi.org/10.1073/pnas.1415123112	journal	March 2015
Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils Wallenstein, Matthew D.; Mcmahon, Shawna K.; Schimel, Joshua P. Global Change Biology, Vol. 15, Issue 7 https://doi.org/10.1111/j.1365-2486.2008.01819.x	journal	July 2009
Soil organic matter quality influences mineralization and GHG emissions in cryosols: a field-based study of sub- to high Arctic Paré, Maxime C.; Bedard-Haughn, Angela Global Change Biology, Vol. 19, Issue 4 https://doi.org/10.1111/gcb.12125	journal	January 2013
Vulnerability of Permafrost Carbon to Climate Change: Implications for the Global Carbon Cycle Schuur, Edward A. G.; Bockheim, James; Canadell, Josep G. BioScience, Vol. 58, Issue 8 https://doi.org/10.1641/B580807	journal	September 2008
Stoichiometry and temperature sensitivity of methanogenesis and CO ₂ production from saturated polygonal tundra in Barrow, Alaska Roy Chowdhury, Taniya; Herndon, Elizabeth M.; Phelps, Tommy J. Global Change Biology, Vol. 21, Issue 2 https://doi.org/10.1111/gcb.12762	journal	November 2014
Exchange of CH4 and N2O in a subarctic heath soil: effects of inorganic N and P and amino acid addition Christensen, T. R.; Michelsen, A.; Jonasson, S. Soil Biology and Biochemistry, Vol. 31, Issue 4 https://doi.org/10.1016/S0038-0717(98)00166-7	journal	April 1999
Sunlight controls water column processing of carbon in arctic fresh waters Cory, R. M.; Ward, C. P.; Crump, B. C. Science, Vol. 345, Issue 6199 https://doi.org/10.1126/science.1253119	journal	August 2014
Climate change and the permafrost carbon feedback Schuur, E. A. G.; McGuire, A. D.; Schädel, C. Nature, Vol. 520, Issue 7546 https://doi.org/10.1038/nature14338	journal	April 2015
Automated Analysis of Electrospray Ionization Fourier Transform Ion Cyclotron Resonance Mass Spectra of Natural Organic Matter Kujawinski, Elizabeth B.; Behn, Mark D. Analytical Chemistry, Vol. 78, Issue 13 https://doi.org/10.1021/ac0600306	journal	July 2006
Soil enzymes in a changing environment: Current knowledge and future directions Burns, Richard G.; DeForest, Jared L.; Marxsen, Jürgen Soil Biology and Biochemistry, Vol. 58 https://doi.org/10.1016/j.soilbio.2012.11.009	journal	March 2013
What is recalcitrant soil organic matter? Kleber, Markus Environmental Chemistry, Vol. 7, Issue 4 https://doi.org/10.1071/EN10006	journal	January 2010
Electrospray and photoionization mass spectrometry for the characterization of organic matter in natural waters: a qualitative assessment: Characterization of organic matter in natural waters Hockaday, William C.; Purcell, Jeremiah M.; Marshall, Alan G. Limnology and Oceanography: Methods, Vol. 7, Issue 1 https://doi.org/10.4319/lom.2009.7.81	journal	January 2009
A pan-Arctic synthesis of CH ₄ and CO ₂ production from anoxic soil incubations Treat, Claire C.; Natali, Susan M.; Ernakovich, Jessica Global Change Biology, Vol. 21, Issue 7 https://doi.org/10.1111/gcb.12875	journal	March 2015
Electrospray: Principles and Practice Gaskell, Simon J. Journal of Mass Spectrometry, Vol. 32, Issue 7, p. 677-688 https://doi.org/10.1002/(SICI)1096-9888(199707)32:7<677::AID-JMS536>3.0.CO;2-G	journal	July 1997
Elemental Composition of HULIS in the Pearl River Delta Region, China: Results Inferred from Positive and Negative Electrospray High Resolution Mass Spectrometric Data Lin, Peng; Rincon, Angela G.; Kalberer, Markus Environmental Science & Technology, Vol. 46, Issue 14 https://doi.org/10.1021/es300285d	journal	June 2012
A decrease in discharge-normalized DOC export by the Yukon River during summer through autumn Striegl, Robert G.; Aiken, George R.; Dornblaser, Mark M. Geophysical Research Letters, Vol. 32, Issue 21 https://doi.org/10.1029/2005GL024413	journal	January 2005
Molecular characterization of dissolved organic matter (DOM) along a river to ocean transect of the lower Chesapeake Bay by ultrahigh resolution electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry Sleighter, Rachel L.; Hatcher, Patrick G. Marine Chemistry, Vol. 110, Issue 3-4 https://doi.org/10.1016/j.marchem.2008.04.008	journal	June 2008
Establishing a Measure of Reproducibility of Ultrahigh-Resolution Mass Spectra for Complex Mixtures of Natural Organic Matter Sleighter, Rachel L.; Chen, Hongmei; Wozniak, Andrew S. Analytical Chemistry, Vol. 84, Issue 21 https://doi.org/10.1021/ac3018026	journal	September 2012
Persistence of soil organic matter as an ecosystem property Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel Nature, Vol. 478, Issue 7367 https://doi.org/10.1038/nature10386	journal	October 2011
Potential carbon release from permafrost soils of Northeastern Siberia Dutta, Koushik; Schuur, E. A. G.; Neff, J. C. Global Change Biology, Vol. 12, Issue 12 https://doi.org/10.1111/j.1365-2486.2006.01259.x	journal	December 2006
Ultrahigh Resolution Mass Spectrometry and Indicator Species Analysis to Identify Marker Components of Soil- and Plant Biomass-Derived Organic Matter Fractions Ohno, Tsutomu; He, Zhongqi; Sleighter, Rachel L. Environmental Science & Technology, Vol. 44, Issue 22 https://doi.org/10.1021/es101089t	journal	November 2010
The effect of permafrost thaw on old carbon release and net carbon exchange from tundra Schuur, Edward A. G.; Vogel, Jason G.; Crummer, Kathryn G. Nature, Vol. 459, Issue 7246 https://doi.org/10.1038/nature08031	journal	May 2009
Indexing Permafrost Soil Organic Matter Degradation Using High-Resolution Mass Spectrometry Mann, Benjamin F.; Chen, Hongmei; Herndon, Elizabeth M. PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0130557	journal	June 2015
Pathways of anaerobic organic matter decomposition in tundra soils from Barrow, Alaska: BIOGEOCHEMISTRY OF ANOXIC ARCTIC TUNDRA Herndon, Elizabeth M.; Mann, Benjamin F.; Roy Chowdhury, Taniya Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 11 https://doi.org/10.1002/2015JG003147	journal	November 2015
Microbes in thawing permafrost: the unknown variable in the climate change equation Graham, David E.; Wallenstein, Matthew D.; Vishnivetskaya, Tatiana A. The ISME Journal, Vol. 6, Issue 4 https://doi.org/10.1038/ismej.2011.163	journal	November 2011
Influence of nitrogen fertilization on methane uptake in temperate forest soils Steudler, P. A.; Bowden, R. D.; Melillo, J. M. Nature, Vol. 341, Issue 6240 https://doi.org/10.1038/341314a0	journal	September 1989
Origin and Sources of Dissolved Organic Matter in Snow on the East Antarctic Ice Sheet Antony, Runa; Grannas, Amanda M.; Willoughby, Amanda S. Environmental Science & Technology, Vol. 48, Issue 11 https://doi.org/10.1021/es405246a	journal	May 2014
The rate of permafrost carbon release under aerobic and anaerobic conditions and its potential effects on climate Lee, Hanna; Schuur, Edward A. G.; Inglett, Kanika S. Global Change Biology, Vol. 18, Issue 2 https://doi.org/10.1111/j.1365-2486.2011.02519.x	journal	September 2011
Identification of Mercury and Dissolved Organic Matter Complexes Using Ultrahigh Resolution Mass Spectrometry Chen, Hongmei; Johnston, Ryne C.; Mann, Benjamin F. Environmental Science & Technology Letters, Vol. 4, Issue 2 https://doi.org/10.1021/acs.estlett.6b00460	journal	December 2016
Advanced Solvent Based Methods for Molecular Characterization of Soil Organic Matter by High-Resolution Mass Spectrometry Tfaily, Malak M.; Chu, Rosalie K.; Tolić, Nikola Analytical Chemistry, Vol. 87, Issue 10 https://doi.org/10.1021/acs.analchem.5b00116	journal	April 2015
Ultrahigh resolution mass spectrometric differentiation of dissolved organic matter isolated by coupled reverse osmosis-electrodialysis from various major oceanic water masses Chen, Hongmei; Stubbins, Aron; Perdue, E. Michael Marine Chemistry, Vol. 164 https://doi.org/10.1016/j.marchem.2014.06.002	journal	August 2014
Substrate quality alters the microbial mineralization of added substrate and soil organic carbon Jagadamma, S.; Mayes, M. A.; Steinweg, J. M. Biogeosciences, Vol. 11, Issue 17 https://doi.org/10.5194/bg-11-4665-2014	journal	January 2014
Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment Yang, Ziming; Yang, Sihang; Van Nostrand, Joy D. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01741	journal	September 2017
The contentious nature of soil organic matter Lehmann, Johannes; Kleber, Markus Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature16069	journal	November 2015
Graphical Method for Analysis of Ultrahigh-Resolution Broadband Mass Spectra of Natural Organic Matter, the Van Krevelen Diagram Kim, Sunghwan; Kramer, Robert W.; Hatcher, Patrick G. Analytical Chemistry, Vol. 75, Issue 20 https://doi.org/10.1021/ac034415p	journal	October 2003
Water-table height and microtopography control biogeochemical cycling in an Arctic coastal tundra ecosystem Lipson, D. A.; Zona, D.; Raab, T. K. Biogeosciences, Vol. 9, Issue 1 https://doi.org/10.5194/bg-9-577-2012	journal	January 2012
Geochemical drivers of organic matter decomposition in arctic tundra soils Herndon, Elizabeth M.; Yang, Ziming; Bargar, John Biogeochemistry, Vol. 126, Issue 3 https://doi.org/10.1007/s10533-015-0165-5	journal	December 2015
The contribution of Fe(III) and humic acid reduction to ecosystem respiration in drained thaw lake basins of the Arctic Coastal Plain: Fe(III) AND HA REDUCTION IN THE ARCTIC Lipson, David A.; Raab, Theodore K.; Goria, Dominic Global Biogeochemical Cycles, Vol. 27, Issue 2 https://doi.org/10.1002/gbc.20038	journal	May 2013
Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM Riley, W. J.; Subin, Z. M.; Lawrence, D. M. Biogeosciences, Vol. 8, Issue 7 https://doi.org/10.5194/bg-8-1925-2011	journal	January 2011
Chemical composition of dissolved organic matter draining permafrost soils Ward, Collin P.; Cory, Rose M. Geochimica et Cosmochimica Acta, Vol. 167 https://doi.org/10.1016/j.gca.2015.07.001	journal	October 2015
From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter Koch, B. P.; Dittmar, T. Rapid Communications in Mass Spectrometry, Vol. 20, Issue 5 https://doi.org/10.1002/rcm.2386	journal	February 2006
Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions Tang, Jinyun; Riley, William J. Nature Climate Change, Vol. 5, Issue 1 https://doi.org/10.1038/nclimate2438	journal	November 2014
The application of electrospray ionization coupled to ultrahigh resolution mass spectrometry for the molecular characterization of natural organic matter Sleighter, Rachel L.; Hatcher, Patrick G. Journal of Mass Spectrometry, Vol. 42, Issue 5 https://doi.org/10.1002/jms.1221	journal	January 2007
Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil Yang, Ziming; Wullschleger, Stan D.; Liang, Liyuan Soil Biology and Biochemistry, Vol. 95 https://doi.org/10.1016/j.soilbio.2015.12.022	journal	April 2016
Multivariate Statistical Approaches for the Characterization of Dissolved Organic Matter Analyzed by Ultrahigh Resolution Mass Spectrometry Sleighter, Rachel L.; Liu, Zhanfei; Xue, Jianhong Environmental Science & Technology, Vol. 44, Issue 19 https://doi.org/10.1021/es1002204	journal	October 2010
Ancient low–molecular-weight organic acids in permafrost fuel rapid carbon dioxide production upon thaw Drake, Travis W.; Wickland, Kimberly P.; Spencer, Robert G. M. Proceedings of the National Academy of Sciences, Vol. 112, Issue 45 https://doi.org/10.1073/pnas.1511705112	journal	October 2015
Methane dynamics regulated by microbial community response to permafrost thaw McCalley, Carmody K.; Woodcroft, Ben J.; Hodgkins, Suzanne B. Nature, Vol. 514, Issue 7523 https://doi.org/10.1038/nature13798	journal	October 2014
Soil-carbon response to warming dependent on microbial physiology Allison, Steven D.; Wallenstein, Matthew D.; Bradford, Mark A. Nature Geoscience, Vol. 3, Issue 5 https://doi.org/10.1038/ngeo846	journal	April 2010
Comparative study of organic matter chemical characterization using negative and positive mode electrospray ionization ultrahigh-resolution mass spectrometry Ohno, Tsutomu; Sleighter, Rachel L.; Hatcher, Patrick G. Analytical and Bioanalytical Chemistry, Vol. 408, Issue 10 https://doi.org/10.1007/s00216-016-9346-x	journal	February 2016
Molecular investigations into a globally important carbon pool: permafrost-protected carbon in Alaskan soils Waldrop, M. P.; Wickland, K. P.; White Iii, R. Global Change Biology https://doi.org/10.1111/j.1365-2486.2009.02141.x	journal	February 2010
Input of easily available organic C and N stimulates microbial decomposition of soil organic matter in arctic permafrost soil Wild, Birgit; Schnecker, Jörg; Alves, Ricardo J. Eloy Soil Biology and Biochemistry, Vol. 75 https://doi.org/10.1016/j.soilbio.2014.04.014	journal	August 2014
Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming Tveit, Alexander Tøsdal; Urich, Tim; Frenzel, Peter Proceedings of the National Academy of Sciences, Vol. 112, Issue 19 https://doi.org/10.1073/pnas.1420797112	journal	April 2015
Soil organic carbon pools in the northern circumpolar permafrost region: SOIL ORGANIC CARBON POOLS Tarnocai, C.; Canadell, J. G.; Schuur, E. A. G. Global Biogeochemical Cycles, Vol. 23, Issue 2 https://doi.org/10.1029/2008GB003327	journal	June 2009
The effects of substrate composition, quantity, and diversity on microbial activity Hernández, Daniel L.; Hobbie, Sarah E. Plant and Soil, Vol. 335, Issue 1-2 https://doi.org/10.1007/s11104-010-0428-9	journal	May 2010

Figures / Tables (6)

Similar Records

Molecular Insights into Arctic Soil Organic Matter Degradation under Warming

Journal Article · Tue Apr 17 00:00:00 EDT 2018 · Environmental Science & Technology · OSTI ID:1433414

Chen, Hongmei; Yang, Ziming; Chu, Rosalie K.; +5 more

Indexing Permafrost Soil Organic Matter Degradation Using High-Resolution Mass Spectrometry

Journal Article · Fri Jun 12 00:00:00 EDT 2015 · PLoS One, 10(6):Article No. e0130557 · OSTI ID:1433414

Mann, Benjamin F.; Chen, Hong-Mei; Herndon, Elizabeth M.; +10 more

Indexing Permafrost Soil Organic Matter Degradation Using High-Resolution Mass Spectrometry

Journal Article · Fri Jun 12 00:00:00 EDT 2015 · PLoS ONE · OSTI ID:1433414

Mann, Benjamin F.; Chen, Hongmei; Herndon, Elizabeth M.; +11 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
54 ENVIRONMENTAL SCIENCES

Title: Molecular Insights into Arctic Soil Organic Matter Degradation under Warming

Citation Formats

References (54)

Figures / Tables (6)

Similar Records

Related Subjects