Advertisement

Biogeochemistry

, Volume 132, Issue 3, pp 307–324 | Cite as

Aggregation controls the stability of lignin and lipids in clay-sized particulate and mineral associated organic matter

  • Gerrit AngstEmail author
  • Kevin E. Mueller
  • Ingrid Kögel-Knabner
  • Katherine H. Freeman
  • Carsten W. Mueller
Article

Abstract

Physical separation of soil into different soil organic matter (SOM) fractions is widely used to identify organic carbon pools that are differently stabilized and have distinct chemical composition. However, the mechanisms underlying these differences in stability and chemical composition are only partly understood. To provide new insights into the stabilization of different chemical compound classes in physically-separated SOM fractions, we assessed shifts in the biomolecular composition of bulk soils and individual particle size fractions that were incubated in the laboratory for 345 days. After the incubation, also the incubated bulk soil was fractionated. The chemical composition of organic matter in bulk soils and fractions was characterized by 13C-CPMAS nuclear magnetic resonance spectroscopy and sequential chemical extraction followed by GC/MS measurements. Plant-derived lipids and lignin were abundant in particulate organic matter (POM) fractions of sand-, silt-, and clay-size and the mineral-bound, clay-sized organic matter. These results indicate that recent conceptualizations of SOM stabilization probably understate the contribution of plant-derived organic matter to stable SOM pools. Although our data indicate that inherent recalcitrance could be important in soils with limited aggregation, organo-mineral interactions and aggregation were responsible for long-term SOM stabilization. In particular, we observed consistently higher concentrations of plant-derived lipids in POM fractions that were incubated individually, where aggregates were disrupted, as compared to those incubated as bulk soil, where aggregates stayed intact. This finding emphasizes the importance of aggregation for the stabilization of less ‘recalcitrant’ biomolecules in the POM fractions. Because also the abundance of lipids and lignin in clay-sized, mineral-associated SOM was substantially influenced by aggregation, the bioavailability of mineral-associated SOM likely increases after the destruction of intact soil structures.

Keywords

Incubation Physical fractionation GC/MS 13C NMR CuO Soil organic matter 

Notes

Acknowledgements

For their help in the laboratory we thank Livia Urbanski and Maria Greiner (TUM Freising, Germany). We also thank David Eissenstat, Professor of Woody Plant Physiology at the Pennsylvania State University, for his assistance, Dr. Werner Häusler (TUM Freising, Germany) for mineralogical analyses, and two anonymous reviewers whose comments helped to greatly improve the quality of the manuscript. The project was generously funded by the Helmholtz Association in the joint virtual institute VH-129 “Centre for Stable Isotope Analysis in Ecosystem Research”, the U.S. National Science Foundation (DEB-0816935, OISE-0754731), the U.S. Department of Energy (Global Change Education Program), the European Association of Organic Geochemists, and the Deutsche Forschungsgemeinschaft (DFG) within the research unit FOR1806 “SUBSOM - The Forgotten Part of Carbon Cycling: Organic Matter Storage and Turnover in Subsoils”.

Supplementary material

10533_2017_304_MOESM1_ESM.tiff (36 mb)
Online Resource 1 13C NMR spectra of initial, bulk soil (incub. bulk), and individually incubated fractions (incub. fract.). Supplementary material 1 (TIFF 36895 kb)

References

  1. Alvarez CR, Alvarez R, Grigera MS, Lavado RS (1998) Associations between organic matter fractions and the active soil microbial biomass. Soil Biol Biochem 30:767–773. doi: 10.1016/S0038-0717(97)00168-5 CrossRefGoogle Scholar
  2. Amelung W, Zech W (1999) Minimisation of organic matter disruption during particle-size fractionation of grassland epipedons. Geoderma 92:73–85. doi: 10.1016/s0016-7061(99)00023-3 CrossRefGoogle Scholar
  3. Amelung W, Brodowski S, Sandhage-Hofmann A, Bol R (2008) Chapter 6 combining biomarker with stable isotope analyses for assessing the transformation and turnover of soil organic matter. Adv Agron 100:155–250CrossRefGoogle Scholar
  4. Angst G, Heinrich L, Kögel-Knabner I, Mueller CW (2016a) The fate of cutin and suberin of decaying leaves, needles and roots: inferences from the initial decomposition of bound fatty acids. Org Geochem 95:81–92. doi: 10.1016/j.orggeochem.2016.02.006 CrossRefGoogle Scholar
  5. Angst G, John S, Mueller CW et al (2016b) Tracing the sources and spatial distribution of organic carbon in subsoils using a multi-biomarker approach. Sci Rep. doi: 10.1038/srep29478 Google Scholar
  6. Angst G, Kögel-Knabner I, Kirfel K et al (2016c) Spatial distribution and chemical composition of soil organic matter fractions in rhizosphere and non-rhizosphere soil under European beech (Fagus sylvatica L.). Geoderma 264:179–187. doi: 10.1016/j.geoderma.2015.10.016 CrossRefGoogle Scholar
  7. Baldock JA, Oades JM, Nelson PN et al (1997) Assessing the extent of decomposition of natural organic materials using solid-state 13C NMR spectroscopy. Soil Res 35:1061–1084. doi: 10.1071/S97004 CrossRefGoogle Scholar
  8. Berg B (2000) Litter decomposition and organic matter turnover in northern forest soils. For Ecol Manage 133:13–22. doi: 10.1016/S0378-1127(99)00294-7 CrossRefGoogle Scholar
  9. Berg B, McClaugherty C (2008) Plant litter: decomposition, humus formation, carbon sequestration, 2nd edn. Springer, BerlinCrossRefGoogle Scholar
  10. Bimüller C, Mueller CW, von Lützow M et al (2014) Decoupled carbon and nitrogen mineralization in soil particle size fractions of a forest topsoil. Soil Biol Biochem 78:263–273. doi: 10.1016/j.soilbio.2014.08.001 CrossRefGoogle Scholar
  11. Blankinship JC, Fonte SJ, Six J, Schimel JP (2016) Plant versus microbial controls on soil aggregate stability in a seasonally dry ecosystem. Geoderma 272:39–50. doi: 10.1016/j.geoderma.2016.03.008 CrossRefGoogle Scholar
  12. Bonanomi G, Incerti G, Giannino F et al (2013) Litter quality assessed by solid state 13C NMR spectroscopy predicts decay rate better than C/N and Lignin/N ratios. Soil Biol Biochem 56:40–48. doi: 10.1016/j.soilbio.2012.03.003 CrossRefGoogle Scholar
  13. Campbell EE, Paustian K (2015) Current developments in soil organic matter modeling and the expansion of model applications: a review. Environ Res Lett 10:123004. doi: 10.1088/1748-9326/10/12/123004 CrossRefGoogle Scholar
  14. Carrington EM, Hernes PJ, Dyda RY et al (2012) Biochemical changes across a carbon saturation gradient: lignin, cutin, and suberin decomposition and stabilization in fractionated carbon pools. Soil Biol Biochem 47:179–190. doi: 10.1016/j.soilbio.2011.12.024 CrossRefGoogle Scholar
  15. Castellano MJ, Mueller KE, Olk DC et al (2015) Integrating plant litter quality, soil organic matter stabilization, and the carbon saturation concept. Glob Chang Biol 21:3200–3209. doi: 10.1111/gcb.12982 CrossRefGoogle Scholar
  16. Chaurasia CS, Williams TD, Judson CM, Hanzlik RP (1995) Quantitation of fatty acids and hydroxy fatty acids by gas chromatography/mass spectrometry. Predictively useful correlations of relative response factors with empirical formula. J Mass Spectrom 30:1018–1022. doi: 10.1002/jms.1190300711 CrossRefGoogle Scholar
  17. Christensen BT (2001) Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–353. doi: 10.1046/j.1365-2389.2001.00417.x CrossRefGoogle Scholar
  18. Clemente JS, Simpson AJ, Simpson MJ (2011) Association of specific organic matter compounds in size fractions of soils under different environmental controls. Org Geochem 42:1169–1180. doi: 10.1016/j.orggeochem.2011.08.010 CrossRefGoogle Scholar
  19. Clemente JS, Simpson MJ, Simpson AJ et al (2013) Comparison of soil organic matter composition after incubation with maize leaves, roots, and stems. Geoderma 192:86–96. doi: 10.1016/j.geoderma.2012.08.007 CrossRefGoogle Scholar
  20. Cotrufo MF, Wallenstein MD, Boot CM et al (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995. doi: 10.1111/gcb.12113 CrossRefGoogle Scholar
  21. Creamer CA, Filley TR, Boutton TW (2013) Long-term incubations of size and density separated soil fractions to inform soil organic carbon decay dynamics. Soil Biol Biochem 57:496–503. doi: 10.1016/j.soilbio.2012.09.007 CrossRefGoogle Scholar
  22. Crow SE, Lajtha K, Filley TR et al (2009) Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Glob Chang Biol 15:2003–2019. doi: 10.1111/j.1365-2486.2009.01850.x CrossRefGoogle Scholar
  23. De Gryze S, Six J, Brits C, Merckx R (2005) A quantification of short-term macroaggregate dynamics: influences of wheat residue input and texture. Soil Biol Biochem 37:55–66. doi: 10.1016/j.soilbio.2004.07.024 CrossRefGoogle Scholar
  24. Ertel JR, Hedges JI (1984) The lignin component of humic substances: distribution among soil and sedimentary humic, fulvic, and base-insoluble fractions. Geochim Cosmochim Acta 48:2065–2074. doi: 10.1016/0016-7037(84)90387-9 CrossRefGoogle Scholar
  25. Ertel JR, Hedges JI (1985) Sources of sedimentary humic substances: vascular plant debris. Geochim Cosmochim Acta 49:2097–2107. doi: 10.1016/0016-7037(85)90067-5 CrossRefGoogle Scholar
  26. Feng X, Simpson MJ (2008) Temperature responses of individual soil organic matter components. J Geophys Res 113(G3). doi: 10.1029/2008JG000743
  27. Feng X, Xu Y, Jaffé R et al (2010) Turnover rates of hydrolysable aliphatic lipids in Duke Forest soils determined by compound specific 13C isotopic analysis. Org Geochem 41:573–579. doi: 10.1016/j.orggeochem.2010.02.013 CrossRefGoogle Scholar
  28. Filley TR, Boutton TW, Liao JD, et al (2008a) Chemical changes to nonaggregated particulate soil organic matter following grassland-to-woodland transition in a subtropical savanna. J Geophys Res Biogeosci. doi: 10.1029/2007JG000564
  29. Filley TR, McCormick MK, Crow SE et al (2008b) Comparison of the chemical alteration trajectory of Liriodendron tulipifera L. leaf litter among forests with different earthworm abundance. J Geophys Res. doi: 10.1029/2007JG000542 Google Scholar
  30. Golchin A, Clarke P, Oades JM (1996) The heterogeneous nature of microbial products as shown by solid-state 13C CP/MAS NMR spectroscopy. Biogeochemistry 34:71–97. doi: 10.1007/BF02180974 CrossRefGoogle Scholar
  31. Goni MA, Hedges JI (1992) Lignin dimers: structures, distribution, and potential geochemical applications. Geochim Cosmochim Acta 56:4025–4043. doi: 10.1016/0016-7037(92)90014-A CrossRefGoogle Scholar
  32. Goñi MA, Montgomery S (2000) Alkaline CuO oxidation with a microwave digestion system: lignin analyses of geochemical samples. Anal Chem 72:3116–3121. doi: 10.1021/ac991316w CrossRefGoogle Scholar
  33. Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307. doi: 10.1016/j.scitotenv.2007.11.013 CrossRefGoogle Scholar
  34. Guggenberger G, Christensen BT, Zech W (1994) Land-use effects on the composition of organic matter in particle-size separates of soil: I. Lignin and carbohydrate signature. Eur J Soil Sci 45:449–458. doi: 10.1111/j.1365-2389.1994.tb00530.x CrossRefGoogle Scholar
  35. Hassink J, Whitmore AP, Kubát J (1997) Size and density fractionation of soil organic matter and the physical capacity of soils to protect organic matter. Eur J Agron 7:189–199. doi: 10.1016/S1161-0301(97)00045-2 CrossRefGoogle Scholar
  36. Hedges JI, Ertel JR (1982) Characterization of lignin by gas capillary chromatography of cupric oxide oxidation products. Anal Chem 54:174–178. doi: 10.1021/ac00239a007 CrossRefGoogle Scholar
  37. Hernes PJ, Kaiser K, Dyda RY, Cerli C (2013) Molecular trickery in soil organic matter: hidden lignin. Environ Sci Technol 47:9077–9085. doi: 10.1021/es401019n CrossRefGoogle Scholar
  38. Ingestad T, Lund A-B (1986) Theory and techniques for steady state mineral nutrition and growth of plants. Scand J For Res 1:439–453. doi: 10.1080/02827588609382436 CrossRefGoogle Scholar
  39. Jansen B, Nierop KGJ, Hageman JA et al (2006) The straight-chain lipid biomarker composition of plant species responsible for the dominant biomass production along two altitudinal transects in the Ecuadorian Andes. Org Geochem 37:1514–1536. doi: 10.1016/j.orggeochem.2006.06.018 CrossRefGoogle Scholar
  40. Kallenbach CM, Grandy A, Frey SD (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun. doi: 10.1038/ncomms13630
  41. Kleber M (2010) What is recalcitrant soil organic matter? Environ Chem 7:320–332. doi: 10.1071/EN10006 CrossRefGoogle Scholar
  42. Klotzbücher T, Kaiser K, Guggenberger G et al (2011) A new conceptual model for the fate of lignin in decomposing plant litter. Ecology 92:1052–1062. doi: 10.1890/i0012-9658-92-5-1052 CrossRefGoogle Scholar
  43. Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162. doi: 10.1016/S0038-0717(01)00158-4 CrossRefGoogle Scholar
  44. Kolattukudy PE (1980) Bio-polyester membranes of plants—cutin and suberin. Science 208:990–1000. doi: 10.1126/science.208.4447.990 CrossRefGoogle Scholar
  45. Kolattukudy PE (1981) Structure, biosynthesis, and biodegradation of cutin and suberin. Annu Rev Plant Physiol Plant Mol Biol 32:539–567. doi: 10.1146/annurev.pp.32.060181.002543 CrossRefGoogle Scholar
  46. Kolattukudy PE, Kronman K, Poulose AJ (1975) Determination of structure and composition of suberin from roots of carrot, parsnip, rutabaga, turnip, red beet and sweet-potato by combined gas-liquid-chromatography and mass-spectrometry. Plant Physiol 55:567–573. doi: 10.1104/pp.55.3.567 CrossRefGoogle Scholar
  47. Krull ES, Baldock JA, Skjemstad JO (2003) Importance of mechanisms and processes of the stabilisation of soil organic matter for modelling carbon turnover. Funct Plant Biol 30:207–222. doi: 10.1071/FP02085 CrossRefGoogle Scholar
  48. Lin LH, Simpson MJ (2016) Enhanced extractability of cutin- and suberin-derived organic matter with demineralization implies physical protection over chemical recalcitrance in soil. Org Geochem 97:111–121. doi: 10.1016/j.orggeochem.2016.04.012 CrossRefGoogle Scholar
  49. Lorenz K, Lal R, Preston CM, Nierop KGJ (2007) Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules. Geoderma 142:1–10. doi: 10.1016/j.geoderma.2007.07.013 CrossRefGoogle Scholar
  50. Marschner B, Brodowski S, Dreves A et al (2008) How relevant is recalcitrance for the stabilization of organic matter in soils? J Plant Nutr Soil Sci 171:91–110. doi: 10.1002/jpln.200700049 CrossRefGoogle Scholar
  51. Mikutta R, Kleber M, Torn MS, Jahn R (2006) Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77:25–56. doi: 10.1007/s10533-005-0712-6 CrossRefGoogle Scholar
  52. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55. doi: 10.1007/s10533-011-9658-z CrossRefGoogle Scholar
  53. Moni C, Rumpel C, Virto I et al (2010) Relative importance of sorption versus aggregation for organic matter storage in subsoil horizons of two contrasting soils. Eur J Soil Sci 61:958–969. doi: 10.1111/j.1365-2389.2010.01307.x CrossRefGoogle Scholar
  54. Mueller CW, Bruggemann N, Pritsch K et al (2009) Initial differentiation of vertical soil organic matter distribution and composition under juvenile beech (Fagus sylvatica L.) trees. Plant Soil 323:111–123. doi: 10.1007/s11104-009-9932-1 CrossRefGoogle Scholar
  55. Mueller CW, Schlund S, Prietzel J et al (2012a) Soil aggregate destruction by ultrasonication increases soil organic matter mineralization and mobility. Soil Sci Soc Am J 76:1634–1643. doi: 10.2136/sssaj2011.0186 CrossRefGoogle Scholar
  56. Mueller KE, Polissar PJ, Oleksyn J, Freeman KH (2012b) Differentiating temperate tree species and their organs using lipid biomarkers in leaves, roots and soil. Org Geochem 52:130–141. doi: 10.1016/j.orggeochem.2012.08.014 CrossRefGoogle Scholar
  57. Mueller CW, Gutsch M, Kothieringer K et al (2014) Bioavailability and isotopic composition of CO 2 released from incubated soil organic matter fractions. Soil Biol Biochem 69:168–178CrossRefGoogle Scholar
  58. Nelson P, Baldock J (2005) Estimating the molecular composition of a diverse range of natural organic materials from solid-state 13C NMR and elemental analyses. Biogeochemistry 72:1–34. doi: 10.1007/s10533-004-0076-3 CrossRefGoogle Scholar
  59. Otto A, Simpson MJ (2006) Evaluation of CuO oxidation parameters for determining the source and stage of lignin degradation in soil. Biogeochemistry 80:121–142. doi: 10.1007/s10533-006-9014-x CrossRefGoogle Scholar
  60. Otto A, Shunthirasingham C, Simpson MJ (2005) A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada. Org Geochem 36:425–448. doi: 10.1016/j.orggeochem.2004.09.008 CrossRefGoogle Scholar
  61. Pisani O, Hills KM, Courtier-Murias D et al (2014) Accumulation of aliphatic compounds in soil with increasing mean annual temperature. Org Geochem 76:118–127. doi: 10.1016/j.orggeochem.2014.07.009 CrossRefGoogle Scholar
  62. Poirier N, Sohi SP, Gaunt JL et al (2005) The chemical composition of measurable soil organic matter pools. Org Geochem 36:1174–1189. doi: 10.1016/j.orggeochem.2005.03.005 CrossRefGoogle Scholar
  63. Prahl FG, Ertel JR, Goni MA et al (1994) Terrestrial organic carbon contributions to sediments on the Washington margin. Geochim Cosmochim Acta 58:3035–3048. doi: 10.1016/0016-7037(94)90177-5 CrossRefGoogle Scholar
  64. Rasse DP, Rumpel C, Dignac M-FF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356. doi: 10.1007/s11104-004-0907-y CrossRefGoogle Scholar
  65. Riederer M, Matzke K, Ziegler F, Kogelknabner I (1993) Occurence, distribution and fate of the lipid plant biopolymers cutin and suberin in temperate forest soils. Org Geochem 20:1063–1076. doi: 10.1016/0146-6380(93)90114-q CrossRefGoogle Scholar
  66. Rumpel C, Eusterhues K, Kogel-Knabner I (2004) Location and chemical composition of stabilized organic carbon in topsoil and subsoil horizons of two acid forest soils. Soil Biol Biochem 36:177–190. doi: 10.1016/j.soilbio.2003.09.005 CrossRefGoogle Scholar
  67. Rumpel C, Eusterhues K, Kögel-Knabner I (2010) Non-cellulosic neutral sugar contribution to mineral associated organic matter in top- and subsoil horizons of two acid forest soils. Soil Biol Biochem 42:379–382. doi: 10.1016/j.soilbio.2009.11.004 CrossRefGoogle Scholar
  68. R Core Team (2015) R: a language and environment for statistic computing, Vienna, Austria.Google Scholar
  69. Schimel DS, Braswell BH, Holland EA et al (1994) Climatic, edaphic, and biotic controls over storage and turnover of carbon in soils. Global Biogeochem Cycles 8:279. doi: 10.1029/94GB00993 CrossRefGoogle Scholar
  70. Schmidt MWI, Torn MS, Abiven S et al (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56. doi: 10.1038/nature10386 CrossRefGoogle Scholar
  71. Schöning I, Morgenroth G, Kögel-Knabner I (2005) O/N-alkyl and alkyl C are stabilised in fine particle size fractions of forest soils. Biogeochemistry 73:475–497. doi: 10.1007/s10533-004-0897-0 CrossRefGoogle Scholar
  72. Schrumpf M, Kaiser K, Guggenberger G et al (2013) Storage and stability of organic carbon in soils as related to depth, occlusion within aggregates, and attachment to minerals. Biogeosciences 10:1675–1691. doi: 10.5194/bg-10-1675-2013 CrossRefGoogle Scholar
  73. Six J, Conant RT, Paul EA, Paustian K (2002) Stabilization mechanisms of soil organic matter: implications for C-saturation of soils. Plant Soil 241:155–176. doi: 10.1023/A:1016125726789 CrossRefGoogle Scholar
  74. Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31. doi: 10.1016/j.still.2004.03.008 CrossRefGoogle Scholar
  75. Sjöberg G, Nilsson SI, Persson T, Karlsson P (2004) Degradation of hemicellulose, cellulose and lignin in decomposing spruce needle litter in relation to N. Soil Biol Biochem 36:1761–1768. doi: 10.1016/j.soilbio.2004.03.010 CrossRefGoogle Scholar
  76. Sollins P, Homann P, Caldwell BA (1996) Stabilization and destabilization of soil organic matter1.pdf. Geoderma 74:65–105. doi: 10.1016/S0016-7061(96)00036-5 CrossRefGoogle Scholar
  77. Spaccini R, Piccolo A, Haberhauer G, Gerzabek MH (2000) Transformation of organic matter from maize residues into labile and humic fractions of three European soils as revealed by 13C distribution and CPMAS-NMR spectra. Eur J Soil Sci 51:583–594. doi: 10.1046/j.1365-2389.2000.00341.x CrossRefGoogle Scholar
  78. Spielvogel S, Prietzel J, Leide J, Riedel M, Zemke J, Kögel-Knabner I (2014) Distribution of cutin and suberin biomarkers under forest trees with different root systems. Plant Soil 381:95–110. doi: 10.1007/s11104-014-2103-z CrossRefGoogle Scholar
  79. Stemmer M, Von Lützow M, Kandeler E et al (1999) The effect of maize straw placement on mineralization of C and N in soil particle size fractions. Eur J Soil Sci 50:73–85. doi: 10.1046/j.1365-2389.1999.00204.x CrossRefGoogle Scholar
  80. Thevenot M, Dignac MF, Rumpel C (2010) Fate of lignins in soils: a review. Soil Biol Biochem 42:1200–1211. doi: 10.1016/j.soilbio.2010.03.017 CrossRefGoogle Scholar
  81. Torn MS, Trumbore SE, Chadwick OA et al (1997) Mineral control of soil organic carbon storage and turnover. Nature 389:170–173. doi: 10.1038/38260 CrossRefGoogle Scholar
  82. von Lützow M, Kögel-Knabner I, Ekschmitt K et al (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur J Soil Sci 57:426–445. doi: 10.1111/j.1365-2389.2006.00809.x CrossRefGoogle Scholar
  83. von Lützow M, Kogel-Knabner I, Ekschmittb K et al (2007) SOM fractionation methods: relevance to functional pools and to stabilization mechanisms. Soil Biol Biochem 39:2183–2207. doi: 10.1016/j.soilbio.2007.03.007 CrossRefGoogle Scholar
  84. Wagai R, Mayer LM, Kitayama K (2009) Nature of the “occluded” low-density fraction in soil organic matter studies: a critical review. J Soil Sci Plant Nutr 55:13–25. doi: 10.1111/j.1747-0765.2008.00356.x CrossRefGoogle Scholar
  85. Ziegler F, Kögel I, Zech W (1986) Alteration of gymnosperm and angiosperm lignin during decomposition in forest humus layers. J Soil Sci Plant Nutr 331:323–331. doi: 10.1002/jpln.19861490309 Google Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Chair of Soil ScienceTechnical University of Munich (TUM)FreisingGermany
  2. 2.United States Department of Agriculture, Agricultural Research ServiceRangeland Resources Research UnitFt. CollinsUSA
  3. 3.Institute for Advanced StudyTechnical University of Munich (TUM)GarchingGermany
  4. 4.Department of GeosciencesPennsylvania State UniversityUniversity ParkUSA
  5. 5.Institute of Soil Biology and SoWa RI, Biology CentreCzech Academy of SciencesČeské BudějoviceCzech Republic

Personalised recommendations