Abstract
Globally, soil organic matter (SOM) contains more than three times as much carbon as either the atmosphere or terrestrial vegetation. Yet it remains largely unknown why some SOM persists for millennia whereas other SOM decomposes readily—and this limits our ability to predict how soils will respond to climate change. Recent analytical and experimental advances have demonstrated that molecular structure alone does not control SOM stability: in fact, environmental and biological controls predominate. Here we propose ways to include this understanding in a new generation of experiments and soil carbon models, thereby improving predictions of the SOM response to global warming.
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References
Fischlin, A. et al. in Climate Change 2007: Impacts, Adaptation and Vulnerability (eds Parry, M. L., Canziani, O. F., Palutikof, J. P., van der Linden, P. J. & Hanson, C. E. ) 211–272 (Cambridge Univ. Press, 2007)
Friedlingstein, P. et al. Climate-carbon cycle feedback analysis: results from the C4MIP model intercomparison. J. Clim. 19, 3337–3353 (2006)A systematic comparison of model predictions of soil carbon response to climate change.
von Lützow, M. & Kögel-Knabner, I. Temperature sensitivity of soil organic matter decomposition—what do we know? Biol. Fertil. Soils 46, 1–15 (2009)A review and outline of research needs about the response of soil organic matter to rising temperatures
Kirschbaum, M. U. F. The temperature dependence of organic-matter decomposition — still a topic of debate. Soil Biol. Biochem. 38, 2510–2518 (2006)
Heimann, M. & Reichstein, M. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451, 289–292 (2008)
Trumbore, S. E. & Czimczik, C. I. An uncertain future for soil carbon. Science 321, 1455–1456 (2008)
Sollins, P., Homann, P. & Caldwell, B. A. Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74, 65–105 (1996)Described mechanisms of SOM stabilization involving environmental controls.
Hedges, J. I. et al. The molecularly-uncharacterized component of nonliving organic matter in natural environments. Org. Geochem. 31, 945–958 (2000)Formulated the fundamental question of why, when organic matter is thermodynamically unstable, does it persist in soils, sometimes for thousands of years?
Hedges, J. I. & Oades, J. M. Comparative organic geochemistries of soils and sediments. Org. Geochem. 27, 319–361 (1997)
Totsche, K. U. et al. Biogeochemical interfaces in soil: the interdisciplinary challenge for soil science. J. Plant Nutr. Soil Sci. 173, 88–99 (2010)
Oades, J. M. The retention of organic matter in soils. Biogeochemistry 5, 35–70 (1988)
Marschner, B. et al. How relevant is recalcitrance for the stabilization of organic matter in soils? J. Plant Nutr. Soil Sci. 171, 91–110 (2008)
Kleber, M. & Johnson, M. G. Advances in understanding the molecular structure of soil organic matter: implications for interactions in the environment. Adv. Agron. 106, 77–142 (2010)
Melillo, J. M., Aber, J. D. & Muratore, J. F. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63, 621–626 (1982)
Amelung, W., Brodowski, S., Sandhage-Hofmann, A. & Bol, R. Combining biomarker with stable isotope analysis for assessing the transformation and turnover of soil organic matter. Adv. Agron. 100, 155–250 (2008)A review including a compilation of the surprisingly rapid and overlapping turnover times of individual molecular compounds previously suspected to have ‘slow’ turnover.
Knorr, M., Frey, S. D. & Curtis, P. S. Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86, 3252–3257 (2005)
Grandy, A. S. & Neff, J. C. Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci. Total Environ. 404, 297–307 (2008)
Ekschmitt, K. et al. Soil-carbon preservation through habitat constraints and biological limitations on decomposer activity. J. Plant Nutr. Soil Sci. 171, 27–35 (2008)
Stevenson, F. J. Humus Chemistry (Wiley, 1994)
Olk, D. C. & Gregorich, E. G. Overview of the symposium proceedings, “Meaningful pools in determining soil carbon and nitrogen dynamics”. Soil Sci. Soc. Am. J. 70, 967–974 (2006)
von Lützow, M. et al. Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions — a review. Eur. J. Soil Sci. 57, 426–445 (2006)
Lehmann, J. et al. Spatial complexity of soil organic matter forms at nanometre scales. Nature Geosci. 1, 238–242 (2008)
Sutton, R. & Sposito, G. Molecular structure in soil humic substances: the new view. Environ. Sci. Technol. 39, 9009–9015 (2005)
Haumaier, L. & Zech, W. Black carbon — possible source of highly aromatic components of soil humic acids. Org. Geochem. 23, 191–196 (1995)
Trompowsky, P. M. et al. Characterization of humic like substances obtained by chemical oxidation of eucalyptus charcoal. Org. Geochem. 36, 1480–1489 (2005)
Preston, C. M. & Schmidt, M. W. I. Black (pyrogenic) carbon: a synthesis of current knowledge and uncertainties with special consideration of boreal regions. Biogeosciences 3, 397–420 (2006)A summary of the current understanding of the formation, properties and fate of fire-residues in natural ecosystems.
Schmidt, M. W. I. & Noack, A. G. Black carbon in soils and sediments: analysis, distribution, implications, and current challenges. Glob. Biogeochem. Cycles 14, 777–794 (2000)
Cohen-Ofri, I., Weiner, L., Boaretto, E., Mintz, G. & Weiner, S. Modern and fossil charcoal: aspects of structure and diagenesis. J. Archaeol. Sci. 33, 428–439 (2006)
Hammes, K., Torn, M. S., Lapenas, A. G. & Schmidt, M. W. I. Centennial black carbon turnover observed in a Russian steppe soil. Biogeosciences 5, 1339–1350 (2008)
Major, J., Lehmann, J., Rondon, M. & Goodale, C. Fate of soil-applied black carbon: downward migration, leaching and soil respiration. Glob. Change Biol. 16, 1366–1379 (2010)
Kim, S., Kaplan, L. A., Benner, R. & Hatcher, P. G. Hydrogen-deficient molecules in natural riverine water samples — evidence for the existence of black carbon in DOM. Mar. Chem. 92, 225–234 (2004)
Dittmar, T. & Paeng, J. A heat-induced molecular signature in marine dissolved organic matter. Nature Geosci. 2, 175–179 (2009)
Ziolkowski, L. A. & Druffel, E. R. M. Aged black carbon identified in marine dissolved organic carbon. Geophys. Res. Lett. 37, L16601 (2010)
Nguyen, B. T., Lehmann, J., Hockaday, W. C., Joseph, S. & Masiello, C. A. Temperature sensitivity of black carbon decomposition and oxidation. Environ. Sci. Technol. 44, 3324–3331 (2010)
Keiluweit, M., Nico, P. S., Johnson, M. G. & Kleber, M. Dynamic molecular structure of plant biomass-derived black carbon (biochar). Environ. Sci. Technol. 44, 1247–1253 (2010)
Liang, B. et al. Stability of biomass-derived black carbon in soils. Geochim. Cosmochim. Acta 72, 6069–6078 (2008)
Cheng, C. H. & Lehmann, J. Ageing of black carbon along a temperature gradient. Chemosphere 75, 1021–1027 (2009)
Lehmann, J. et al. Australian climate-carbon cycle feedback reduced by soil black carbon. Nature Geosci. 1, 832–835 (2008)
Brodowski, S., John, B., Flessa, H. & Amelung, W. Aggregate-occluded black carbon in soil. Eur. J. Soil Sci. 57, 539–546 (2006)
Rasse, D. P., Rumpel, C. & Dignac, M. F. Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269, 341–356 (2005)
Kong, A. Y. Y. & Six, J. Tracing root vs. residue carbon into soils from conventional and alternative cropping systems. Soil Sci. Soc. Am. J. 74, 1201–1210 (2010)
Balesdent, J. & Balabane, M. Major contribution of roots to soil carbon storage inferred from maize cultivated soils. Soil Biol. Biochem. 28, 1261–1263 (1996)
Mendez-Millan, M., Dignac, M. F., Rumpel, C., Rasse, D. P. & Derenne, S. Molecular dynamics of shoot vs. root biomarkers in an agricultural soil estimated by natural abundance 13C labelling. Soil Biol. Biochem. 42, 169–177 (2010)
Kramer, C. et al. Recent (4 year old) leaf litter is not a major source of microbial carbon in a temperate forest mineral soil. Soil Biol. Biochem. 42, 1028–1037 (2010)
Bird, J. A., Kleber, M. & Torn, M. S. 13C and 15N stabilization dynamics in soil organic matter fractions during needle and fine root decomposition. Org. Geochem. 39, 465–477 (2008)
Bird, J. A. & Torn, M. S. Fine roots vs. needles: A comparison of 13C and 15N dynamics in a ponderosa pine forest soil. Biogeochemistry 79, 361–382 (2006)
Godbold, D. L. et al. Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 281, 15–24 (2006)
Fontaine, S. et al. Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450, 277–280 (2007)
Kuzyakov, Y. Priming effects: interactions between living and dead organic matter. Soil Biol. Biochem. 42, 1363–1371 (2010)
Ågren, G. I., Bosatta, E. & Magill, A. H. Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128, 94–98 (2001)
Janssens, I. A. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nature Geosci. 3, 315–322 (2010)
Chabbi, A., Kogel-Knabner, I. & Rumpel, C. Stabilised carbon in subsoil horizons is located in spatially distinct parts of the soil profile. Soil Biol. Biochem. 41, 256–261 (2009)
Jobbágy, E. G. & Jackson, R. B. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol. Appl. 10, 423–436 (2000)
Trumbore, S. E., Davidson, E. A., de Camargo, P. B., Nepstad, D. C. & Martinelli, L. A. Belowground cycling of carbon in forests and pastures of Eastern Amazonia. Glob. Biogeochem. Cycles 9, 515–528 (1995)
Rumpel, C. & Kögel-Knabner, I. Deep soil organic matter — a key but poorly understood component of terrestrial C cycle. Plant Soil 338, 143–158 (2011)A comprehensive overview of key challenges to quantitative understanding of deep soil carbon.
Kalbitz, K., Schwesig, D., Rethemeyer, J. & Matzner, E. Stabilization of dissolved organic matter by sorption to the mineral soil. Soil Biol. Biochem. 37, 1319–1331 (2005)
Torn, M. S. et al. Organic carbon and carbon isotopes in modern and 100-year-old soil archives of the Russian steppe. Glob. Change Biol. 8, 941–953 (2002)
Fierer, N., Allen, A. S., Schimel, J. P. & Holden, P. A. Controls on microbial CO2 production: a comparison of surface and subsurface soil horizons. Glob. Change Biol. 9, 1322–1332 (2003)
Kramer, C. & Gleixner, G. Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biol. Biochem. 40, 425–433 (2008)
Tarnocai, C. et al. Soil organic carbon pools in the northern circumpolar permafrost region. Glob. Biogeochem. Cycles 23 GB2023 10.1029/2008GB003327 (2009)
Schuur, E. A. G. et al. The effect of permafrost thaw on old carbon release and net carbon exchange from tundra. Nature 459, 556–559 (2009)
Schuur, E. A. G. et al. Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. Bioscience 58, 701–714 (2008)
Nowinski, N. S., Taneva, L., Trumbore, S. E. & Welker, J. M. Decomposition of old organic matter as a result of deeper active layers in a snow depth manipulation experiment. Oecologia 163, 785–792 (2010)
Mack, M. C., Schuur, E. A. G., Bret-Harte, M. S., Shaver, G. R. & Chapin, F. S. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431, 440–443 (2004)
Nowinski, N. S., Trumbore, S. E., Schuur, E. A. G., Mack, M. C. & Shaver, G. R. Nutrient addition prompts rapid destabilization of organic matter in an arctic tundra ecosystem. Ecosystems 11, 16–25 (2008)
Striegl, R. G., Aiken, G. R., Dornblaser, M. M., Raymond, P. A. & Wickland, K. P. A decrease in discharge-normalized DOC export by the Yukon River during summer through autumn. Geophys. Res. Lett. 32 L21413 10.1029/2005GL024413 (2005)
Kawahigashi, M., Kaiser, K., Rodionov, A. & Guggenberger, G. Sorption of dissolved organic matter by mineral soils of the Siberian forest tundra. Glob. Change Biol. 12, 1868–1877 (2006)
Raes, J. & Bork, P. Molecular eco-systems biology: towards an understanding of community function. Nature Rev. Microbiol. 6, 693–699 (2008)
Morales, S. E. & Holben, W. E. Linking bacterial identities and ecosystem processes: can 'omic' analyses be more than the sum of their parts? FEMS Microbiol. Ecol. 75, 2–16 (2011)
Kögel-Knabner, I. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol. Biochem. 34, 139–162 (2002)
McGuire, K. L. & Treseder, K. K. Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol. Biochem. 42, 529–535 (2010)
von Mering, C. et al. Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315, 1126–1130 (2007)
Kleber, M. What is recalcitrant soil organic matter? Environ. Chem. 7, 320–332 (2010)
Manzoni, S. & Porporato, A. Soil carbon and nitrogen mineralization: theory and models across scales. Soil Biol. Biochem. 41, 1355–1379 (2009)
Kucharik, C. J. et al. Measurements and modeling of carbon and nitrogen cycling in agroecosystems of southern Wisconsin: potential for SOC sequestration during the next 50 years. Ecosystems 4, 237–258 (2001)
Jenkinson, D. S. The turnover of organic carbon and nitrogen in soil. Phil. Trans. R. Soc. Lond. 329, 361–368 (1990)
Parton, W. J., Ojima, D. S., Cole, C. V. & Schimel, D. S. in Quantitative Modeling of Soil Forming Processes (eds Bryant, R. B. & Arnold, R. W. ) 147–167 (Special Publication, Soil Science Society of America, 1994)
Thornton, P. E. & Rosenbloom, N. A. Ecosystem model spin-up: estimating steady state conditions in a coupled terrestrial carbon and nitrogen cycle model. Ecol. Model. 189, 25–48 (2005)
Khvorostyanov, D. V., Krinner, G., Ciais, P., Heimann, M. & Zimov, S. A. Vulnerability of permafrost carbon to global warming. Part I: model description and role of heat generated by organic matter decomposition. Tellus B 60, 250–264 (2008)
Arrhenius, S. Über die Reaktionsgeschwindigkeit bei der Inversion von Rohrzucker durch Säuren. Z. Phys. Chem. 4, 226–248 (1889)
Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006)
Knorr, W., Prentice, I. C., House, J. I. & Holland, E. A. Long-term sensitivity of soil carbon turnover to warming. Nature 433, 298–301 (2005)
Kirschbaum, M. U. F. The temperature dependence of organic matter decomposition: seasonal temperature variations turn a sharp short-term temperature response into a more moderate annually averaged response. Glob. Change Biol. 16, 2117–2129 (2010)
Fang, C., Smith, P., Moncrieff, J. B. & Smith, J. U. Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 433, 57–59 (2005)
Craine, J. M., Fierer, N. & McLauchlan, K. K. Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nature Geosci. 3, 854–857 (2010)
Lorenz, K., Lal, R., Preston, C. M. & Nierop, K. G. J. Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules. Geoderma 142, 1–10 (2007)
Thevenot, M., Dignac, M. F. & Rumpel, C. Fate of lignins in soils: a review. Soil Biol. Biochem. 42, 1200–1211 (2010)
Lehmann, J. A handful of carbon. Nature 447, 143–144 (2007)
Sachs, J. et al. Monitoring the world's agriculture. Nature 466, 558–560 (2010)
Richter, D. D., Hofmockel, M., Callaham, M. A., Powlson, D. S. & Smith, P. Long-term soil experiments: keys to managing Earth's rapidly changing ecosystems. Soil Sci. Soc. Am. J. 71, 266–279 (2007)
Amundson, R. & Jenny, H. The place of humans in the state factor theory of ecosystems and their soils. Soil Sci. 151, 99–109 (1991)
Amstalden van Hove, E. R., Smith, D. F. & Heeren, R. M. A. A concise review of mass spectrometry imaging. J. Chromatogr. A 1217, 3946–3954 (2010)
Herrmann, A. M. et al. Nano-scale secondary ion mass spectrometry — a new analytical tool in biogeochemistry and soil ecology: A review article. Soil Biol. Biochem. 39, 1835–1850 (2007)
Ranjard, L. et al. Biogeography of soil microbial communities: a review and a description of the ongoing French national initiative. Agron. Sustain. Dev. 30, 359–365 (2010)
Pascault, N. et al. In situ dynamics of microbial communities during decomposition of wheat, rape and alfalfa residues. Microb. Ecol. 60, 816–828 (2010)
Xu, T. F. Incorporating aqueous reaction kinetics and biodegradation into TOUGHREACT: applying a multiregion model to hydrobiogeochemical transport of denitrification and sulfate reduction. Vadose Zone J. 7, 305–315 (2008)
Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Rev. Microbiol. 8, 593–599 (2010)
Sollins, P., Swanston, C. & Kramer, M. Stabilization and destabilization of soil organic matter — a new focus. Biogeochemistry 85, 1–7 (2007)
Torn, M. S., Trumbore, S. E., Chadwick, O. A., Vitousek, P. M. & Hendricks, D. M. Mineral control of soil organic carbon storage and turnover. Nature 389, 170–173 (1997)
Kelleher, B. P. & Simpson, A. J. Humic substances in soils: are they really chemically distinct? Environ. Sci. Technol. 40, 4605–4611 (2006)
Acknowledgements
The European Science Foundation Network MOLTER sponsored the workshop at which the idea for this Perspective was conceived. Support for M.W.I.S. and M.S.T. was also provided by the US Department of Energy (contract no. DE-AC02-05CH11231).
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M.W.I.S. coordinated the MOLTER-sponsored workshop mentioned above; the ideas were developed by all authors. M.W.I.S. and M.S.T. participated actively and equally in the writing of the manuscript and the drafting of the figures. All authors provided input into the drafting and the final version of the manuscript.
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Schmidt, M., Torn, M., Abiven, S. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011). https://doi.org/10.1038/nature10386
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DOI: https://doi.org/10.1038/nature10386
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