, Volume 140, Issue 1, pp 81–92 | Cite as

Microbial and plant-derived compounds both contribute to persistent soil organic carbon in temperate soils

  • Pierre BarréEmail author
  • Katell Quénéa
  • Alix Vidal
  • Lauric Cécillon
  • Bent T. Christensen
  • Thomas Kätterer
  • Andy Macdonald
  • Léo Petit
  • Alain F. Plante
  • Folkert van Oort
  • Claire Chenu


Our study tests the emerging paradigm that biochemical recalcitrance does not affect substantially long-term (50 years) SOC persistence. We analyzed the molecular composition of SOC in archived soils originating from four European long-term bare fallow experiments (Askov, Rothamsted, Versailles and Ultuna). The soils had been collected after various periods (up to 53 years) under bare fallow. With increasing duration of bare fallow without new organic inputs, the relative abundance of cutin- and suberin-derived compounds declined substantially, and the abundance of lignin-derived compounds was close to zero. Conversely, the relative abundance of plant-derived long-chain alkanes remained almost constant or increased during the bare fallow period. The relative abundance of N-containing compounds, considered to be abundant in SOC derived from microbial activity, increased consistently illustrating that microbial turnover of SOC continues even when plant inputs are stopped. The persistence of the different families of plant-derived compounds differed markedly over the scale of half a century, which may be ascribed to their contrasting chemical characteristics and recalcitrance, or to differences in their interactions with the soil mineral matrix, and likely some combination since chemical composition drives the degree of mineral association. Using soil from this unique set of long-term bare fallow experiments, we provide direct evidence that multi-decadal scale persistent SOC is enriched in microbe-derived compounds but also includes a substantial fraction of plant-derived compounds.


TMAH-Py–GC–MS Long-term bare fallow Plant-derived compounds Soil organic carbon persistence 



The INSU EC2CO program is acknowledged for financial support (CARACAS Project). We thank Rothamsted Research and the Lawes Agricultural Trust for access to archived samples and the BBSRC for support under the Institute National Capabilities program grant. Related information and data can be found in the electronic Rothamsted Archive ( The Danish contribution was financially supported by The Ministry of Environment and Food. The Swedish contribution was supported by the Faculty of Natural Resources and Agriculture at the Swedish University of Agricultural Sciences. We thank the two reviewers for their constructive comments on the manuscript.

Supplementary material

10533_2018_475_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 19 kb)
10533_2018_475_MOESM2_ESM.docx (23 kb)
Supplementary material 2 (DOCX 23 kb)


  1. Amelung W, Brodowski S, Sandhage-Hofmann A, Bol R (2008) Combining biomarker with stable isotope analysis for assessing the transformation and turnover of soil organic matter. Adv Agron 100:155–250CrossRefGoogle Scholar
  2. Armas-Herrera CM, Dignac MF, Rumpel C, Arbelo CD, Chabbi A (2016) Management effects on composition and dynamics of cutin and suberin in topsoil under agricultural use. Eur J Soil Sci 67:360–373CrossRefGoogle Scholar
  3. Balabane M, Plante AF (2004) Aggregation and carbon storage in silty soil using physical fractionation techniques. Eur J Soil Sci 55:415–427CrossRefGoogle Scholar
  4. Barré P, Eglin T, Christensen BT, Ciais P, Houot S, Kätterer T, van Oort F, Peylin P, Poulton PR, Romanenkov V, Chenu C (2010) Quantifying and isolating stable soil organic carbon using long-term bare fallow experiments. Biogeosciences 7:3839–3850CrossRefGoogle Scholar
  5. Barré P, Plante AF, Cécillon L, Lutfalla S, Baudin F, Bernard S, Christensen BT, Eglin T, Fernandez JM, Houot S, Kätterer T, Le Guillou C, Macdonald A, van Oort F, Chenu C (2016) The energetic and chemical signatures of persistent soil organic matter. Biogeochem 130:1–12CrossRefGoogle Scholar
  6. Buurman P, Roscoe R (2011) Different chemical composition of free light, occluded light and extractable SOM fractions in soils of Cerrado and tilled and untilled fields, Minas Gerais, Brazil: a pyrolysis–GC/MS study. Eur J Soil Sci 62:253–266CrossRefGoogle Scholar
  7. Carr AS, Boom A, Chase BM, Meadows ME, Roberts ZE, Britton MN, Cumming AM (2013) Biome-scale characterization and differentiation of semi-arid and arid zone soil organic matter compositions using pyrolysis–GC/MS analysis. Geoderma 200:189–201CrossRefGoogle Scholar
  8. Chefetz B, Chen Y, Clapp CE, Hatcher PG (2000) Characterization of organic matter in soils by thermochemolysis using tetramethylammonium hydroxide (TMAH). Soil Sci Soc Am J 64:283–289CrossRefGoogle Scholar
  9. Christensen BT (2001) Physical fractionation of soil and structural and functional complexity in organic matter turnover. Eur J Soil Sci 52:345–353CrossRefGoogle Scholar
  10. Clifford DJ, Carson DM, McKinney DE, Bortiatynski JM, Hatcher PG (1995) A new rapid technique for the characterization of lignin in vascular plants: thermochemolysis with tetramethylammonium hydroxide (TMAH). Org Geochem 23:169–175CrossRefGoogle Scholar
  11. Coward EK, Ohno T, Plante AF (2018) Adsorption and molecular fractionation of dissolved organic matter on iron-bearing mineral matrices of varying crystallinity. Environ Sci Technol 52(3):1036–1044CrossRefGoogle Scholar
  12. Del Río JC, Hatcher PG (1998) Analysis of aliphatic biopolymers using thermochemolysis with tetramethylammonium hydroxide (TMAH) and gas chromatography–mass spectrometry. Org Geochem 29:1441–1451CrossRefGoogle Scholar
  13. Derenne S, Quenea K (2015) Analytical pyrolysis as a tool to probe soil organic matter. J Anal Appl Pyrolysis 111:108–120CrossRefGoogle Scholar
  14. Dignac M-F, Bahri H, Rumpel C, Rasse DP, Bardoux G, Balesdent J, Girardin C, Chenu C, Mariotti A (2005) 13C natural abundance as a tool to study the dynamics of lignin monomers in soil: an appraisal at the Closeaux experimental field (France). Geoderma 128:3–17CrossRefGoogle Scholar
  15. Fabbri D, Helleur R (1999) Characterization of the tetramethylammonium hydroxide thermochemolysis products of carbohydrates. J Anal Appl Pyrolysis 49:277–293CrossRefGoogle Scholar
  16. Grandy SG, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307CrossRefGoogle Scholar
  17. Grasset L, Amblès A (1998) Aliphatic lipids released from a soil humin after enzymatic degradation of cellulose. Org Geochem 29:893–897CrossRefGoogle Scholar
  18. Haddix ML, Magrini-Bair K, Evans RJ, Conant RT, Wallenstein MD, Morris SJ, Calderon F, Paul EA (2016) Progressing towards more quantitative analytical pyrolysis of soil organic matter using molecular beam mass spectroscopy of whole soils and added standards. Geoderma 283:88–100CrossRefGoogle Scholar
  19. Han J, Calvin M (1969) Hydrocarbon distribution of algae and bacteria, and microbiological activity in sediments. Proc Natl Acad Sci USA 64:436–443CrossRefGoogle Scholar
  20. Hofmann A, Heim A, Christensen BT, Miltner A, Gehre M, Schmidt MWI (2009) Lignin dynamics in two 13C-labelled arable soils during 18 years. Eur J Soil Sci 60:250–257CrossRefGoogle Scholar
  21. Kallenbach CM, Frey SD, Grandy SG (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630CrossRefGoogle Scholar
  22. Kelleher BP, Simpson MJ, Simpson AJ (2006) Assessing the fate and transformation of plant residues in the terrestrial environment using HR-MAS NMR spectroscopy. Geochim Cosmochim Acta 70:4080–4094CrossRefGoogle Scholar
  23. Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162CrossRefGoogle Scholar
  24. Kolattukudy PE (1980) Biopolyester membranes of plants: cutin and suberin. Science 208:990–1000CrossRefGoogle Scholar
  25. Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68CrossRefGoogle Scholar
  26. Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105CrossRefGoogle Scholar
  27. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochem 111:41–55CrossRefGoogle Scholar
  28. Mitchell PJ, Simpson AJ, Soong R, Oren A, Chefetz B, Simpson MJ (2013) Solution-state NMR investigation of the sorptive fractionation of dissolved organic matter by alkaline mineral soils. Environ Chem 10:333–340CrossRefGoogle Scholar
  29. Nierop KG (2001) Temporal and vertical organic matter differentiation along a vegetation succession as revealed by pyrolysis and thermally assisted hydrolysis and methylation. J Anal Appl Pyrolysis 61:111–132CrossRefGoogle Scholar
  30. Nierop KGJ, van Bergen PF, Buurman P, van Lagen B (2005) NaOH and Na4P2O7 extractable organic mater in two allophanic volcanic ash soils of the Azores Islands—a pyrolysis gc/ms study. Geoderma 127:36–51CrossRefGoogle Scholar
  31. Oliveira DMS, Schellenkens J, Cerri CEP (2016) Molecular characterization of soil organic matter from native vegetation-pasture-sugarcane transitions in Brazil. Sci Total Environ 548–549:450–462CrossRefGoogle Scholar
  32. Otto A, Simpson MJ (2006) Sources and composition of hydrolysable aliphatic lipids and phenols in soils from western Canada. Org Geochem 37:385–407CrossRefGoogle Scholar
  33. 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 36:425–448CrossRefGoogle Scholar
  34. Quénéa K, Largeau C, Derenne S, Spaccini R, Bardoux G, Mariotti A (2006) Molecular and isotopic study of lipids in particle size fractions of a sandy cultivated soil (Cestas cultivation sequence, southwest France): sources, degradation, and comparison with Cestas forest soil. Org Geochem 37:20–44CrossRefGoogle Scholar
  35. Quénéa K, Mathieu J, Derenne S (2012) Soil lipids from accelerated solvent extraction: influence of temperature and solvent on extract composition. Org Geochem 44:45–52CrossRefGoogle Scholar
  36. Riederer M, Matzke K, Ziegler F, Kögel-Knabner I (1993) Occurrence, distribution and fate of the lipid plant biopolymers cutin and suberin in temperate forest soils. Org Geochem 20:1063–1076CrossRefGoogle Scholar
  37. Rieley G, Collier RJ, Jones DM, Eglinton G, Eakin PA, Fallick AE (1991) Sources of sedimentary lipids deduced from stable carbon-isotope analyses of individual compounds. Nature 352(6334):425CrossRefGoogle Scholar
  38. Schellekens J, Barberá GG, Buurman P, Pérez-Jordà G, Martínez-Cortizas A (2013) Soil organic matter dynamics in Mediterranean A-horizons—the use of analytical pyrolysis to ascertain land-use history. J Anal Appl Pyrolysis 104:287–298CrossRefGoogle Scholar
  39. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter. Nature 478:49–56CrossRefGoogle Scholar
  40. Sollins P, Kramer MG, Swanston C, Lajtha K, Filley T, Aufdenkampe AK, Wagai R, Bowden RD (2009) Sequential density fractionation across soils of contrasted mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96:209–231CrossRefGoogle Scholar
  41. Stockmann U, Adams MA, Crawford JW, Field DJ et al (2013) The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agr Ecosyst Environ 164:80–99CrossRefGoogle Scholar
  42. Vancampenhout K, Wouters K, De Vos B, Buurman P, Swennen R, Deckers J (2009) Differences in chemical composition of soil organic matter in natural ecosystems from different climatic regions—a pyrolysis-GC/MS study. Soil Biol Biochem 41:568–579CrossRefGoogle Scholar
  43. Vidal A, Quenea K, Alexis M, Derenne S (2016) Molecular fate of root and shoot litter on incorporation and decomposition in earthworm casts. Org Geochem 101:1–10CrossRefGoogle Scholar
  44. Wannigama GP, Volkman JK, Gillan FT, Nichols PD, Johns RB (1981) A comparison of lipid components of the fresh and dead leaves and pneumatophores of the mangrove Avicennia marina. Phytochemistry 20:659–666CrossRefGoogle Scholar
  45. Wickings K, Grandy SG, Reed SC, Cleveland CC (2012) The origin of litter chemical complexity during decomposition. Ecol Lett 15:1180–1188CrossRefGoogle Scholar
  46. Wiesenberg GLB, Gocke M, Kuzyakov Y (2010) Fast incorporation of root-derived lipids and fatty acids into soil—evidence from a short term multiple pulse labelling experiment. Org Geochem 41:1049–1055CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Pierre Barré
    • 1
    Email author
  • Katell Quénéa
    • 2
  • Alix Vidal
    • 3
  • Lauric Cécillon
    • 4
  • Bent T. Christensen
    • 5
  • Thomas Kätterer
    • 6
  • Andy Macdonald
    • 7
  • Léo Petit
    • 2
  • Alain F. Plante
    • 8
  • Folkert van Oort
    • 9
  • Claire Chenu
    • 9
  1. 1.Laboratoire de Géologie de l’ENS - PSL Research University – CNRS UMR8538ParisFrance
  2. 2.Sorbonne Universités, UPMC Univ Paris 06, CNRS, EPHE, UMR 7619 MetisParis Cedex 05France
  3. 3.Lehrstuhl für BodenkundeTU MünchenFreisingGermany
  4. 4.Université Grenoble Alpes, Irstea, UR EMGRSt-Martin-d’HèresFrance
  5. 5.Department of AgroecologyAarhus UniversityTjeleDenmark
  6. 6.Department of EcologySwedish University of Agricultural SciencesUppsalaSweden
  7. 7.Department of Sustainable Agriculture SciencesRothamsted ResearchHarpendenUK
  8. 8.Earth and Environmental ScienceUniversity of PennsylvaniaPhiladelphiaUSA
  9. 9.AgroParisTech – INRA, UMR 1402 ECOSYSThiverval GrignonFrance

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