What is recalcitrant soil organic matter?

Markus Kleber

doi:10.1071/EN10006

RESEARCH ARTICLE

Previous Next Contents Vol 7(4)

What is recalcitrant soil organic matter?

Markus Kleber

+ Author Affiliations

- Author Affiliations

Department of Crop and Soil Science, Oregon State University, 3017 Agriculture and Life Sciences Building, Corvallis, OR 97331, USA. Email: markus.kleber@oregonstate.edu

Environmental Chemistry 7(4) 320-332 https://doi.org/10.1071/EN10006
Submitted: 20 January 2010 Accepted: 1 June 2010 Published: 20 August 2010

Environmental context. On a global scale, soils store more carbon than plants or the atmosphere. The cycling of this vast reservoir of reduced carbon is closely tied to variations in environmental conditions, but robust predictions of climate–carbon cycle feedbacks are hampered by a lack of mechanistic knowledge regarding the sensitivity of organic matter decomposition to rising temperatures. This text provides a critical discussion of the practice to conceptualise parts of soil organic matter as intrinsically resistant to decomposition or ‘recalcitrant’.

Abstract. The understanding that some natural organic molecules can resist microbial decomposition because of certain molecular properties forms the basis of the biogeochemical paradigm of ‘intrinsic recalcitrance’. In this concept paper I argue that recalcitrance is an indeterminate abstraction whose semantic vagueness encumbers research on terrestrial carbon cycling. Consequently, it appears to be advantageous to view the perceived ‘inherent resistance’ to decomposition of some forms of organic matter not as a material property, but as a logistical problem constrained by (i) microbial ecology; (ii) enzyme kinetics; (iii) environmental drivers; and (iv) matrix protection. A consequence of this view would be that the frequently observed temperature sensitivity of the decomposition of organic matter must result from factors other than intrinsic molecular recalcitrance.

Acknowledgements

I am indebted to Noah Fierer for sharing the data for Fig. 3 and to Joan Sandeno for language edits to the final version of the manuscript. Marco Keiluweit, Peter S. Nico and Dave D. Myrold provided helpful comments on earlier versions of the manuscript. Three anonymous reviewers are acknowledged for their constructive suggestions to improve the manuscript.

References

[1] E. G. Jobbágy , R. B. Jackson , The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol. Appl. 2000 , 10, 423.
        | Crossref | GoogleScholarGoogle Scholar |

[2] C. Tarnocai , J. G. Canadell , E. A. G. Schuur , P. Kuhry , G. Mazhitova , S. Zimov , Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochem. Cy. 2009 , 23, GB2023.
        | Crossref | GoogleScholarGoogle Scholar |

[3] M. Heimann , M. Reichstein , Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 2008 , 451, 289.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[4] M. S. Torn , J. Harte , Missing feedbacks, asymmetric uncertainties, and the underestimation of future warming. Geophys. Res. Lett. 2006 , 33, L10703.
        | Crossref | GoogleScholarGoogle Scholar |

[5] M. Scheffer , V. Brovkin , P. M. Cox , Positive feedback between global warming and atmospheric CO₂ concentration inferred from past climate change. Geophys. Res. Lett. 2006 , 33, L10702.
        | Crossref | GoogleScholarGoogle Scholar |

[6] E. Dorrepaal , S. Toet , R. S. P. van Logtestijn , E. Swart , M. J. van de Weg , T. V. Callaghan , R. Aerts , Carbon respiration from subsurface peat accelerated by climate warming in the subarctic. Nature 2009 , 460, 616.
        | Crossref | GoogleScholarGoogle Scholar |

[7] M. von Lützow , I. Kögel-Knabner , Temperature sensitivity of soil organic matter decomposition-what do we know? Biol. Fertil. Soils 2009 , 46, 1.
        | Crossref | GoogleScholarGoogle Scholar |

[8] C. M. Fang , P. Smith , J. B. Moncrieff , J. U. Smith , Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 2005 , 433, 57.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[9] C. Fang , P. Smith , J. U. Smith , Is resistant soil organic matter more sensitive to temperature than the labile organic matter? Biogeosciences 2006 , 3, 65.
        | Crossref | GoogleScholarGoogle Scholar |

[10] M. Reichstein , T. Katterer , O. Andren , P. Ciais , E. D. Schulze , W. Cramer , D. Papale , R. Valentini , Temperature sensitivity of decomposition in relation to soil organic matter pools: critique and outlook. Biogeosciences 2005 , 2, 317.
        | Crossref | GoogleScholarGoogle Scholar |

[11] M. Reichstein , J. A. Subke , A. C. Angeli , J. D. Tenhunen , Does the temperature sensitivity of decomposition of soil organic matter depend upon water content, soil horizon, or incubation time? Glob. Change Biol. 2005 , 11, 1754.
        | Crossref | GoogleScholarGoogle Scholar |

[12] F. Conen , J. Leifeld , B. Seth , C. Alewell , Warming mineralises young and old soil carbon equally. Biogeosciences 2006 , 3, 515.
        | Crossref | GoogleScholarGoogle Scholar |

[13] Smith P., Fang C. M., Dawson J. J. C., Moncrieff J. B., Impact of global warming on soil organic carbon, in Advances in Agronomy, Vol. 97 2008, pp. 1–43 (Elsevier Academic Press Inc: San Diego, CA).

[14] E. A. Davidson , I. A. Janssens , Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 2006 , 440, 165.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[15] E. Bosatta , G. I. Agren , Soil organic matter quality interpreted thermodynamically. Soil Biol. Biochem. 1999 , 31, 1889.
        | Crossref | GoogleScholarGoogle Scholar |

[16] B. Marschner , S. Brodowski , A. Dreves , G. Gleixner , A. Gude , P. M. Grootes , U. Hamer , A. Heim , et al. How relevant is recalcitrance for the stabilization of organic matter in soils? J. Plant Nutr. Soil Sc. 2008 , 171, 91.
        | Crossref | GoogleScholarGoogle Scholar |

[17] D. L. Wixon , T. C. Balser , Complexity, climate change and soil carbon: a systems approach to microbial temperature response. Syst. Res. Behav. Sci. 2009 , 26, 601.
        | Crossref | GoogleScholarGoogle Scholar |

[18] M. Alexander , Biodegradation of chemicals of environmental concern. Science 1981 , 211, 132.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[19] P. Sollins , P. Homann , B. A. Caldwell , Stabilization and destabilization of soil organic matter: Mechanisms and controls. Geoderma 1996 , 74, 65.
        | Crossref | GoogleScholarGoogle Scholar |

[20] J. A. Baldock , J. O. Skjemstad , Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org. Geochem. 2000 , 31, 697.
        | Crossref | GoogleScholarGoogle Scholar |

[21] Himmel M. E., Picataggio S. K., Chapter 1: Our challenge is to acquire deeper understanding of biomass recalcitrance and conversion, in Biomass Recalcitrance – Deconstructing the Plant Cell Wall for Bioenergy (Ed. Himmel M. E.) 2008 (Wiley-Blackwell: Chichester).

[22] J. Balesdent , S. Recous , The residence times of C, and the potential for C storage in some French cultivated soils. Can. J. Soil Sci. 1997 , 77, 187.


[23] R. T. Conant , R. A. Drijber , M. L. Haddix , W. J. Parton , E. A. Paul , A. F. Plante , J. Six , J. M. Steinweg , Sensitivity of organic matter decomposition to warming varies with its quality. Glob. Change Biol. 2008 , 14, 868.
        | Crossref | GoogleScholarGoogle Scholar |

[24] R. T. Conant , J. M. Steinweg , M. L. Haddix , E. A. Paul , A. F. Plante , J. Six , Experimental warming shows that decomposition temperature sensitivity increases with soil organic matter recalcitrance. Ecology 2008 , 89, 2384.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[25] S. Trumbore , Radiocarbon and soil carbon dynamics. Annu. Rev. Earth Planet. Sci. 2009 , 37, 47.
        | Crossref | GoogleScholarGoogle Scholar |

[26] M. von Lützow , I. Kögel-Knabner , K. Ekschmitt , E. Matzner , G. Guggenberger , B. Marschner , H. Flessa , Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions – a review. Eur. J. Soil Sci. 2006 , 57, 426.
        | Crossref | GoogleScholarGoogle Scholar |

[27] Brady N. C., Weil R. R., The Nature and Properties of Soils 2008 (Prentice Hall: Upper Saddle River, NJ).

[28] H.-R. Schulten , M. Schnitzer , Chemical model structures for soil organic matter and soils. Soil Sci. 1997 , 162, 115.
        | Crossref | GoogleScholarGoogle Scholar |

[29] R. Swift , Macromolecular properties of soil humic substances: fact, fiction and opinion. Soil Sci. 1999 , 164, 790.
        | Crossref | GoogleScholarGoogle Scholar |

[30] A. Piccolo , The supramolecular structure of humic substances. Soil Sci. 2001 , 166, 810.
        | Crossref | GoogleScholarGoogle Scholar |

[31] R. Sutton , G. Sposito , Molecular structure in soil humic substances: the new view. Environ. Sci. Technol. 2005 , 39, 9009.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[32] K. Lorenz , R. Lal , C. M. Preston , K. G. J. Nierop , Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules. Geoderma 2007 , 142, 1.
        | Crossref | GoogleScholarGoogle Scholar |

[33] G. L. B. Wiesenberg , J. Schwarzbauer , M. W. I. Schmidt , L. Schwark , Source and turnover of organic matter in agricultural soils derived from n-alkane/n-carboxylic acid compositions and C-isotope signatures. Org. Geochem. 2004 , 35, 1371.


[34] R. Bol , N. Poirier , J. Balesdent , G. Gleixner , Molecular turnover time of soil organic matter in particle-size fractions of an arable soil. Rapid Commun. Mass Spectrom. 2009 , 23, 2551.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[35] M. Alexander , Biodegradation: problems of molecular recalcitrance and microbial fallibility. Adv. Appl. Microbiol. 1965 , 7, 35.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[36] E. S. Krull , J. A. Baldock , J. O. Skjemstad , Importance of mechanisms and processes of the stabilization of soil organic matter for modelling carbon turnover. Funct. Plant Biol. 2003 , 30, 207.
        | Crossref | GoogleScholarGoogle Scholar |

[37] Parton W. J., Ojima D., Cole C. V., Schimel D. S., A general model for soil organic matter dynamics: Sensitivity to litter chemistry, texture and management, in Quantitative Modeling of Soil Forming Processes (Eds Bryant R., Arnold R.) 1994, Special Publication 39, pp. 147–167 (SSSA: Madison, WI).

[38] D. S. Jenkinson , The turnover of organic carbon and nitrogen in soil. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1990 , 329, 361.
        | Crossref | GoogleScholarGoogle Scholar |

[39] T. Dittmar , G. Kattner , Recalcitrant dissolved organic matter in the ocean: major contribution of small amphiphilics. Mar. Chem. 2003 , 82, 115.
        | Crossref | GoogleScholarGoogle Scholar |

[40] T. Dittmar , J. Paeng , A heat-induced molecular signature in marine dissolved organic matter. Nature Geosci. 2009 , 2, 175.
        | Crossref | GoogleScholarGoogle Scholar |

[41] Frimmel F. H., Abbt-Braun G., Heumann K. G., Hock B., Luedemann H.-D., Spiteller M., Refractory Organic Substances in the Environment 2002 (Wiley-WCH: Weinheim).

[42] ASTM, C71 – 08 Standard Terminology Relating to Refractories 2009 (American Society for Testing and Materials: Philadelphia, PA).

[43] A. Tietema , D. VanDam , Calculating microbial carbon and nitrogen transformations in acid forest litter with ¹⁵N enrichment and dynamic simulation modelling. Soil Biol. Biochem. 1996 , 28, 953.
        | Crossref | GoogleScholarGoogle Scholar |

[44] Alexander M., Introduction to Soil Microbiology 1961 (Wiley: New York).

[45] M. Alexander , Biochemical ecology of soil microorganisms. Annu. Rev. Microbiol. 1964 , 18, 217.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[46] L. M. Mayer , The inertness of being organic. Mar. Chem. 2004 , 92, 135.
        | Crossref | GoogleScholarGoogle Scholar |

[47] K. Ekschmitt , E. Kandeler , C. Poll , A. Brune , F. Buscot , M. Friedrich , G. Gleixner , A. Hartmann , et al. Soil-carbon preservation through habitat constraints and biological limitations on decomposer activity. J. Plant Nutr. Soil Sc. 2008 , 171, 27.
        | Crossref | GoogleScholarGoogle Scholar |

[48] K. Ekschmitt , M. Liu , S. Vetter , O. Fox , V. Wolters , Strategies used by soil biota to overcome soil organic matter stability – why is dead organic matter left over in the soil? Geoderma 2005 , 128, 167.
        | Crossref | GoogleScholarGoogle Scholar |

[49] W. J. Parton , D. S. Schimel , C. V. Cole , D. S. Ojima , Analysis of factors controlling soil organic matter levels in Great Plains grasslands. Soil Sci. Soc. Am. J. 1987 , 51, 1173.
        | Crossref |

[50] Y. S. Feng , Fundamental considerations of soil organic carbon dynamics: a new theoretical framework. Soil Sci. 2009 , 174, 467.
        | Crossref | GoogleScholarGoogle Scholar |

[51] Stott D. E., Martin J. P., Synthesis and degradation of natural and synthetic humic materials in soils, in Humic Substances in Soil and Crop Sciences: Selected Readings (Eds P. MacCarthy, C. E. Clapp, R. L. Malcolm, P. R. Bloom) 1990, pp. 37–63 (American Society of Agronomy, Inc.: Madison, WI).

[52] G. I. Ågren , E. Bosatta , Quality: A bridge between theory and experiment in soil organic matter studies. Oikos 1996 , 76, 522.
        | Crossref | GoogleScholarGoogle Scholar |

[53] C. Fang , P. Smith , J. U. Smith , A simple equation for simulating C decomposition in a multi-component pool of soil organic matter. Eur. J. Soil Sci. 2005 , 56, 815.


[54] J. Six , R. T. Conant , E. A. Paul , K. Paustian , Stabilization mechanisms of soil organic matter: Implications for C-saturation of soils. Plant Soil 2002 , 241, 155.
        | Crossref | GoogleScholarGoogle Scholar |

[55] Swift M. J., Heal O. W., Anderson J. M., Decomposition in Terrestrial Ecosystems 1979 (University of California Press: Los Angeles).

[56] I. Kögel-Knabner , The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol. Biochem. 2002 , 34, 139.
        | Crossref | GoogleScholarGoogle Scholar |

[57] Sanderman J., Amundson R., Biogeochemistry of Decomposition and Detrital Processing 2005 (Elsevier Amsterdam: Boston, MA).

[58] J. D. Aber , J. M. Melillo , C. A. McClaugherty , Predicting long-term patterns of mass-loss, nitrogen dynamics, and soil organic matter formation from initial litter chemistry in temperate forest ecosystems. Can. J. Bot. 1990 , 68, 2201.
        | Crossref | GoogleScholarGoogle Scholar |

[59] B. R. Taylor , C. E. Prescott , W. J. F. Parsons , D. Parkinson , Substrate control of litter decomposition in four Rocky Mountain coniferous forests. Can. J. Bot. 1991 , 69, 2242.
        | Crossref | GoogleScholarGoogle Scholar |

[60] W. L. Silver , R. K. Miya , Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 2001 , 129, 407.


[61] R. Hatfield , R. S. Fukushima , Can lignin be accurately measured? Crop Sci. 2005 , 45, 832.
        | Crossref | GoogleScholarGoogle Scholar |

[62] Waksman S. A., Humus. Origin, Chemical Composition and Importance in Nature 1936 (Williams and Wilkins: Baltimore, MD).

[63] J. P. Martin , K. Haider , Microbial activity in relation to soil humus formation. Soil Sci. 1971 , 111, 54.
        | Crossref | GoogleScholarGoogle Scholar |

[64] J. P. Martin , H. Zunino , P. Peirano , M. Caiozzi , K. Haider , Decomposition of ¹⁴C-labeled lignins, model humic acid polymers, and funal melanins in allophanic soils. Soil Biol. Biochem. 1982 , 14, 289.
        | Crossref | GoogleScholarGoogle Scholar |

[65] K. Haider , J. P. Martin , Decomposition of specifically C₁₄ labeled benzoic and cinnamic acid derivatives in soil. Soil Sci. Soc. Am. J. 1975 , 39, 657.
        | Crossref |

[66] K. Haider , J. Trojanowski , Decomposition of specifically C-14-labeled phenols and dehydropolymers of coniferyl alcohol as models for lignin degradation by soft and white rot fungi. Arch. Microbiol. 1975 , 105, 33.
        | Crossref | GoogleScholarGoogle Scholar |

[67] Essington M. E., Soil and Water Chemistry 2003 (CRC Press: Boca Raton, FL).

[68] N. Fierer , J. M. Craine , K. McLauchlan , J. P. Schimel , Litter quality and the temperature sensitivity of decomposition. Ecology 2005 , 86, 320.
        | Crossref | GoogleScholarGoogle Scholar |

[69] Gutfreund H., Kinetics for the Life Sciences 1995 (Cambridge University Press: Cambridge, UK).

[70] C. M. Fang , P. Smith , J. B. Moncrieff , J. U. Smith , Corrigendum: Similar response of labile and resistant soil organic matter pools to changes in temperature. Nature 2005 , 436, 881.
        | Crossref | GoogleScholarGoogle Scholar |

[71] E. A. Davidson , I. A. Janssens , Y. Q. Luo , On the variability of respiration in terrestrial ecosystems: moving beyond Q₁₀. Glob. Change Biol. 2006 , 12, 154.
        | Crossref | GoogleScholarGoogle Scholar |

[72] X. J. Feng , M. J. Simpson , Temperature responses of individual soil organic matter components. J. Geophys. Res. 2008 , 113, G03036.
        | Crossref | GoogleScholarGoogle Scholar |

[73] N. Fierer , B. P. Colman , J. P. Schimel , R. B. Jackson , Predicting the temperature dependence of microbial respiration in soil: a continental-scale analysis. Global Biogeochem. Cy. 2006 , 20, GB3026.
        | Crossref | GoogleScholarGoogle Scholar |

[74] J. I. Hedges , G. Eglinton , P. G. Hatcher , D. L. Kirchman , C. Arnosti , S. Derenne , R. P. Evershed , I. Kögel-Knabner , et al. The molecularly-uncharacterized component of nonliving organic matter in natural environments. Org. Geochem. 2000 , 31, 945.
        | Crossref | GoogleScholarGoogle Scholar |

[75] Schlesinger W. H., Biogeochemistry – an Analysis of Global Change 1997 (Academic Press: Amsterdam).

[76] Dickerson R. E., Geis I., Chemistry, Matter and the Universe – An Integrated Approach to General Chemistry 1976 (W. A. Benjamin, Inc.: Menlo Park, CA).

[77] I. J. Glasspool , D. Edwards , L. Axe , Charcoal in the Silurian as evidence for the earliest wildfire. Geology 2004 , 32, 381.
        | Crossref | GoogleScholarGoogle Scholar |

[78] S. Derenne , C. Largeau , A review of some important families of refractory macromolecules: composition, origin and fate in soils and sediments. Soil Sci. 2001 , 166, 833.
        | Crossref | GoogleScholarGoogle Scholar |

[79] Huang P. M., Hardie A. G., Formation mechanisms of humic substances in the environment, in Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems (Eds N. Senesi, B. Xing, P. M. Huang) 2009, pp. 41–109 (Wiley: Hoboken, NJ).

[80] Baldock J. A., Nelson P. N., Soil organic matter, in Handbook of Soil Science (Ed. M. E. Sumner) 2000, pp. B25–B84 (CRC Press: Boca Raton, FL).

[81] M. Kleber , M. G. Johnson , Advances in understanding the molecular structure of soil organic matter: implications for interactions in the environment. Adv. Agron. 2010 , 106, 77.
        | Crossref | GoogleScholarGoogle Scholar |

[82] Haider K., Martin J. P., Filip Z., Humus biochemistry, in Soil Biochemistry (Eds E. A. Paul, A. D. McLaren) 1975, Vol. 4, pp. 195–244 (Marcel Dekker, Inc.: New York).

[83] Wershaw R. L., Evaluation of Conceptual Models of Natural Organic Matter (Humus) From a Consideration of the Chemical and Biochemical Processes of Humification. Scientific Investigations Report 2004–5121 2004 (US Geological Survey: Reston, VA).

[84] J. Lehmann , D. Solomon , J. Kinyangi , L. Dathe , S. Wirick , C. Jacobsen , Spatial complexity of soil organic matter forms at nanometre scales. Nature Geosci. 2008 , 1, 238.
        | Crossref | GoogleScholarGoogle Scholar |

[85] B. P. Kelleher , A. J. Simpson , Humic substances in soils: are they really chemically distinct? Environ. Sci. Technol. 2006 , 40, 4605.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |

[86] M. Tatzber , M. Stemmer , H. Spiegel , C. Katzlberger , F. Zehetner , G. Haberhauer , K. Roth , E. Garcia-Garcia , M. H. Gerzabek , Decomposition of carbon-14-labeled organic amendments and humic acids in a long-term field experiment. Soil Sci. Soc. Am. J. 2009 , 73, 744.
        | Crossref | GoogleScholarGoogle Scholar |

[87] W. Amelung , I. Lobe , C. C. Du Preez , Fate of microbial residues in sandy soils of the South African Highveld as influenced by prolonged arable cropping. Eur. J. Soil Sci. 2002 , 53, 29.
        | Crossref | GoogleScholarGoogle Scholar |

[88] R. Kiem , I. Koegel-Knabner , Contribution of lignin and polysaccharides to the refractory carbon pool in C-depleted arable soils. Soil Biol. Biochem. 2003 , 35, 101.
        | Crossref | GoogleScholarGoogle Scholar |

[89] H. Knicker , Stabilization of N-compounds in soil and organic-matter-rich sediments – what is the difference? Mar. Chem. 2004 , 92, 167.
        | Crossref | GoogleScholarGoogle Scholar |

[90] J. P. Schimel , M. N. Weintraub , The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol. Biochem. 2003 , 35, 549.
        | Crossref | GoogleScholarGoogle Scholar |

[91] T. Wutzler , M. Reichstein , Colimitation of decomposition by substrate and decomposers – a comparison of model formulations. Biogeosciences 2008 , 5, 749.
        | Crossref | GoogleScholarGoogle Scholar |

[92] S. Manzoni , A. Porporato , Soil carbon and nitrogen mineralization: theory and models across scales. Soil Biol. Biochem. 2009 , 41, 1355.
        | Crossref | GoogleScholarGoogle Scholar |

[93] D. G. Neary , C. C. Klopatek , L. F. DeBano , P. F. Ffolliott , Fire effects on belowground sustainability: a review and synthesis. For. Ecol. Manage. 1999 , 122, 51.
        | Crossref | GoogleScholarGoogle Scholar |

[94] M. I. Bird , Fire in the earth sciences. Episodes 1997 , 20, 223.


[95] H. Knicker , How does fire affect the nature and stability of soil organic nitrogen and carbon? A review. Biogeochemistry 2007 , 85, 91.
        | Crossref | GoogleScholarGoogle Scholar |

[96] A. Miltner , W. Zech , Effects of minerals on the transformation of organic matter during simulated fire-induced pyrolysis. Org. Geochem. 1997 , 26, 175.
        | Crossref | GoogleScholarGoogle Scholar |

[97] C. I. Czimczik , C. M. Preston , M. W. I. Schmidt , E. D. Schulze , How surface fire in Siberian Scots pine forests affects soil organic carbon in the forest floor: stocks, molecular structure, and conversion to black carbon (charcoal). Global Biogeochem. Cy. 2003 , 17, 1020.
        | Crossref | GoogleScholarGoogle Scholar |

[98] J. A. Baldock , R. J. Smernik , Chemical composition and bioavailability of thermally altered Pinus resinosa (Red pine) wood. Org. Geochem. 2002 , 33, 1093.
        | Crossref | GoogleScholarGoogle Scholar |

[99] U. Hamer , B. Marschner , S. Brodowski , W. Amelung , Interactive priming of black carbon and glucose mineralisation. Org. Geochem. 2004 , 35, 823.
        | Crossref | GoogleScholarGoogle Scholar |

[100] K. Hammes , M. S. Torn , A. G. Lapenas , M. W. I. Schmidt , Centennial black carbon turnover observed in a Russian steppe soil. Biogeosciences 2008 , 5, 1339.
        | Crossref | GoogleScholarGoogle Scholar |

[101] C. H. Cheng , J. Lehmann , M. H. Engelhard , Natural oxidation of black carbon in soils: changes in molecular form and surface charge along a climosequence. Geochim. Cosmochim. Acta 2008 , 72, 1598.
        | Crossref | GoogleScholarGoogle Scholar |

[102] C.-H. Cheng , J. Lehmann , J. E. Thies , S. D. Burton , Stability of black carbon in soils across a climatic gradient. J. Geophys. Res. 2008 , 113, G02027.
        | Crossref | GoogleScholarGoogle Scholar |

[103] C.-H. Cheng , J. Lehmann , J. E. Thies , S. D. Burton , M. H. Engelhard , Oxidation of black carbon by biotic and abiotic processes. Org. Geochem. 2006 , 37, 1477.
        | Crossref | GoogleScholarGoogle Scholar |

[104] M. I. Bird , C. Moyo , E. M. Veenendaal , J. Lloyd , P. Frost , Stability of elemental carbon in a savanna soil. Global Biogeochem. Cy. 1999 , 13, 923.
        | Crossref | GoogleScholarGoogle Scholar |

[105] M. Ohlson , B. Dahlberg , T. Okland , K. J. Brown , R. Halvorsen , The charcoal carbon pool in boreal forest soils. Nature Geosci. 2009 , 2, 692.
        | Crossref | GoogleScholarGoogle Scholar |

[106] C. A. Campbell , E. A. Paul , D. A. Rennie , K. J. McCallum , Applicability of the carbon-dating method of analysis to soil humus studies. Soil Sci. 1967 , 104, 217.
        | Crossref | GoogleScholarGoogle Scholar |

[107] J. A. Baldock , J. M. Oades , P. N. Nelson , T. M. Skene , A. Golchin , P. Clarke , Assessing the extent of decomposition of natural organic materials using solid-state ¹³C NMR spectroscopy. Aust. J. Soil Res. 1997 , 35, 1061.
        | Crossref | GoogleScholarGoogle Scholar |

[108] C. A. Masiello , W. C. Hockaday , M. E. Gallagher , Organic carbon oxidation state (C-ox): a new proxy for the Earth’s C and O cycles. Geochimica Et Cosmochimica Acta 2007 , 71, A633.


[109] W. C. Hockaday , C. A. Masiello , J. T. Randerson , R. J. Smernik , J. A. Baldock , O. A. Chadwick , J. W. Harden , Measurement of soil carbon oxidation state and oxidative ratio by ¹³C nuclear magnetic resonance. J. Geophys. Res. 2009 , 114, G02014.
        | Crossref | GoogleScholarGoogle Scholar |

[110] C. Rumpel , K. Eusterhues , I. Kogel-Knabner , Location and chemical composition of stabilized organic carbon in topsoil and subsoil horizons of two acid forest soils. Soil Biol. Biochem. 2004 , 36, 177.
        | Crossref | GoogleScholarGoogle Scholar |

[111] C. Rumpel , A. Seraphin , M. O. Goebel , G. Wiesenberg , F. Gonzales-Vila , J. Bachmann , L. Schwark , W. Michaelis , A. Mariotti , I. Kögel-Knabner , Alkyl C and hydrophobicity in B and C horizons of an acid forest soil. J. Plant Nutr. Soil Sc. 2004 , 167, 685.
        | Crossref | GoogleScholarGoogle Scholar |

[112] A. J. Sexstone , N. P. Revsbech , T. B. Parkin , J. M. Tiedje , Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci. Soc. Am. J. 1985 , 49, 645.
        | Crossref |

[113] G. E. M. van der Lee , B. de Winder , W. Bouten , A. Tietema , Anoxic microsites in Douglas fir litter. Soil Biol. Biochem. 1999 , 31, 1295.
        | Crossref | GoogleScholarGoogle Scholar |

[114] H. E. Hartnett , R. G. Keil , J. I. Hedges , A. H. Devol , Influence of oxygen exposure time on organic carbon preservation in continental margin sediments. Nature 1998 , 391, 572.
        | Crossref | GoogleScholarGoogle Scholar |

[115] R. G. Keil , A. F. Dickens , T. Arnarson , B. L. Nunn , A. H. Devol , What is the oxygen exposure time of laterally transported organic matter along the Washington margin? Mar. Chem. 2004 , 92, 157.
        | Crossref | GoogleScholarGoogle Scholar |

[116] J. I. Hedges , R. G. Keil , Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar. Chem. 1995 , 49, 81.
        | Crossref | GoogleScholarGoogle Scholar |

[117] Hayakawa S. I., Language in Thought and Action 1949 (Harcourt, Brace and Company, Inc: New York).

[118] Torn M. S., Swanston C. W., Castanha C., Trumbore S. E., Storage and turnover of organic matter in soil, in Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems (Eds N. Senesi, B. Xing, P. M. Huang) 2009, pp. 219–272 (Wiley: Hoboken, NJ).

[119] P. D. Falloon , P. Smith , Modelling refractory soil organic matter. Biol. Fertil. Soils 2000 , 30, 388.
        | Crossref | GoogleScholarGoogle Scholar |

[120] J. M. Talbot , S. D. Allison , K. K. Treseder , Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct. Ecol. 2008 , 22, 955.
        | Crossref | GoogleScholarGoogle Scholar |

[121] C. A. Masiello , M. E. Gallagher , J. T. Randerson , R. M. Deco , O. A. Chadwick , Evaluating two experimental approaches for measuring ecosystem carbon oxidation state and oxidative ratio. J. Geophys. Res. – Biogeosciences 2008 , 113, G03010.
        | Crossref | GoogleScholarGoogle Scholar |

[122] S. E. Trumbore , S. H. Zheng , Comparison of fractionation methods for soil organic matter C-14 analysis. Radiocarbon 1996 , 38, 219.


[123] H. Knicker , P. G. Hatcher , Sequestration of organic nitrogen in the sapropel from Mangrove Lake, Bermuda. Org. Geochem. 2001 , 32, 733.
        | Crossref | GoogleScholarGoogle Scholar |

[124] K. Eusterhues , C. Rumpel , M. Kleber , I. Kogel-Knabner , Stabilisation of soil organic matter by interactions with minerals as revealed by mineral dissolution and oxidative degradation. Org. Geochem. 2003 , 34, 1591.
        | Crossref | GoogleScholarGoogle Scholar |

[125] K. Haase , K. Wantzen , Analysis and decomposition of condensed tannins in tree leaves. Environ. Chem. Lett. 2008 , 6, 71.
        | Crossref | GoogleScholarGoogle Scholar |

[126] N. Poirier , S. Derenne , J. N. Rouzaud , C. Largeau , A. Mariotti , J. Balesdent , J. Maquet , Chemical structure and sources of the macromolecular, resistant, organic fraction isolated from a forest soil (Lacadee, south-west France). Org. Geochem. 2000 , 31, 813.
        | Crossref | GoogleScholarGoogle Scholar |

[127] O. E. Craig , M. J. Collins , The removal of protein from mineral surfaces: implications for residue analysis of archaeological materials. J. Archaeol. Sci. 2002 , 29, 1077.
        | Crossref | GoogleScholarGoogle Scholar |

[128] M. Keiluweit , P. S. Nico , M. G. Johnson , M. Kleber , Dynamic molecular structure of plant biomass-derived black carbon (Biochar). Environ. Sci. Technol. 2010 , 44, 1247.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |