Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Molecular trade-offs in soil organic carbon composition at continental scale

Abstract

The molecular composition of soil organic carbon remains contentious. Microbial-, plant- and fire-derived compounds may each contribute, but whether they vary predictably among ecosystems remains unclear. Here we present carbon functional groups and molecules from a diverse spectrum of North American surface mineral soils, collected primarily from the National Ecological Observatory Network and quantified by nuclear magnetic resonance spectroscopy and a molecular mixing model. We find that soils vary widely in relative contributions of carbohydrate, lipid, protein, lignin and char-like carbon, but each compound class has similar overall abundance. Ninety percent of the variance in carbon composition can be explained by three principal component axes representing a trade-off between lignin and protein, a trade-off between carbohydrate and char, and lipids. Reactive aluminium, crystalline iron oxides and pH plus overlying organic horizon thickness—predictors that are all related to climate—best explain variation along each respective axis. Together, our data point to continental-scale trade-offs in soil carbon molecular composition that are linked to environmental and geochemical variables known to predict carbon mass concentrations. Controversies regarding the genesis of soil carbon and its potential responses to global change can be partially reconciled by considering diverse ecosystem properties that drive complementary persistence mechanisms.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Box plots of carbon abundance as the fraction of total SOC in each sample.
Fig. 2: Rotated principal components analysis of SOC molecules.
Fig. 3: Heatmap of correlations (r) between SOC molecules and biogeochemical predictors.
Fig. 4: Parsimonious structural equation models of SOC molecular composition.
Fig. 5: Conceptual model of three-dimensional trade-offs in SOC composition linked to complementary persistence mechanisms as supported by our data.

Similar content being viewed by others

Data availability

Summarized NMR data are available in the Supplementary Information, and raw NMR spectra data and sample biogeochemical characteristics are available in the Environmental Data Initiative digital repository: https://doi.org/10.6073/pasta/2284825ecb8460f056ae5b0e7d355cc8.

Code availability

R scripts used for post-processing data are available in the Environmental Data Initiative digital repository: https://doi.org/10.6073/pasta/2284825ecb8460f056ae5b0e7d355cc8.

References

  1. Baldock, J. A., Masiello, C. A., Gélinas, Y. & Hedges, J. I. Cycling and composition of organic matter in terrestrial and marine ecosystems. Mar. Chem. 92, 39–64 (2004).

    Google Scholar 

  2. Sutton, R. & Sposito, G. Molecular structure in soil humic substances: the new view. Environ. Sci. Technol. 39, 9009–9015 (2005).

    Google Scholar 

  3. Lehmann, J. & Kleber, M. The contentious nature of soil organic matter. Nature 528, 60–68 (2015).

    Google Scholar 

  4. Baldock, J. A. et al. Assessing the extent of decomposition of natural organic materials using solid-state 13C NMR spectroscopy. Aust. J. Soil Res. 35, 1061–1084 (1997).

    Google Scholar 

  5. Mahieu, N., Randall, E. W. & Powlson, D. S. Statistical analysis of published carbon-13 CPMAS NMR spectra of soil organic matter. Soil Sci. Soc. Am. J. 63, 307–319 (1999).

    Google Scholar 

  6. 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).

    Google Scholar 

  7. Baldock, J. A. et al. Aspects of the chemical structure of soil organic materials as revealed by solid-state 13C NMR spectroscopy. Biogeochemistry 16, 1–42 (1992).

    Google Scholar 

  8. Ahmad, R., Nelson, P. N. & Kookana, R. S. The molecular composition of soil organic matter as determined by 13C NMR and elemental analyses and correlation with pesticide sorption. Eur. J. Soil Sci. 57, 883–893 (2006).

    Google Scholar 

  9. Rasmussen, C. et al. Beyond clay: towards an improved set of variables for predicting soil organic matter content. Biogeochemistry 137, 297–306 (2018).

    Google Scholar 

  10. Cotrufo, M. F., Ranalli, M. G., Haddix, M. L., Six, J. & Lugato, E. Soil carbon storage informed by particulate and mineral-associated organic matter. Nat. Geosci. 12, 989–994 (2019).

    Google Scholar 

  11. Wagai, R. et al. Linking temperature sensitivity of soil organic matter decomposition to its molecular structure, accessibility, and microbial physiology. Glob. Change Biol. 19, 1114–1125 (2013).

    Google Scholar 

  12. Waksman, S. A. & Iyer, K. R. N. Contribution to our knowledge of the chemical nature and origin of humus: I. on the synthesis of the “humus nucleus”. Soil Sci. 34, 43–69 (1932).

    Google Scholar 

  13. Kirk, T. K. & Farrell, R. L. Enzymatic "combustion": the microbial degradation of lignin. Annu. Rev. Microbiol. 41, 465–501 (1987).

    Google Scholar 

  14. Amelung, W., Brodowski, S., Sandhage-Hofmann, A. & Bol, R. in Advances in Agronomy Vol. 100 (ed. Sparks, D. L.) 155–250 (Elsevier, 2008).

  15. Thevenot, M., Dignac, M.-F. & Rumpel, C. Fate of lignins in soils: a review. Soil Biol. Biochem. 42, 1200–1211 (2010).

    Google Scholar 

  16. Bosatta, E. & Ågren, G. I. Soil organic matter quality interpreted thermodynamically. Soil Biol. Biochem. 31, 1889–1891 (1999).

    Google Scholar 

  17. Miltner, A., Bombach, P., Schmidt-Brücken, B. & Kästner, M. SOM genesis: microbial biomass as a significant source. Biogeochemistry 111, 41–55 (2011).

    Google Scholar 

  18. Cotrufo, M. F., Wallenstein, M. D., Boot, C. M., Denef, K. & Paul, E. 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. Change Biol. 19, 988–995 (2013).

    Google Scholar 

  19. Kallenbach, C. M., Frey, S. D. & Grandy, A. S. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7, 13630 (2016).

    Google Scholar 

  20. Ma, T. et al. Divergent accumulation of microbial necromass and plant lignin components in grassland soils. Nat. Commun. 9, 3480 (2018).

    Google Scholar 

  21. Liang, C., Amelung, W., Lehmann, J. & Kästner, M. Quantitative assessment of microbial necromass contribution to soil organic matter. Glob. Change Biol. 25, 3578–3590 (2019).

    Google Scholar 

  22. Khan, K. S., Mack, R., Castillo, X., Kaiser, M. & Joergensen, R. G. Microbial biomass, fungal and bacterial residues, and their relationships to the soil organic matter C/N/P/S ratios. Geoderma 271, 115–123 (2016).

    Google Scholar 

  23. Malik, A. A. et al. Land use driven change in soil pH affects microbial carbon cycling processes. Nat. Commun. 9, 3591 (2018).

    Google Scholar 

  24. Córdova, S. C. et al. Plant litter quality affects the accumulation rate, composition, and stability of mineral-associated soil organic matter. Soil Biol. Biochem. 125, 115–124 (2018).

    Google Scholar 

  25. Huang, W. et al. Enrichment of lignin-derived carbon in mineral-associated soil organic matter. Environ. Sci. Technol. 53, 7522–7531 (2019).

    Google Scholar 

  26. Wan, D. et al. Iron oxides selectively stabilize plant-derived polysaccharides and aliphatic compounds in agricultural soils. Eur. J. Soil Sci. 70, 1153–1163 (2019).

    Google Scholar 

  27. Hernes, P. J., Kaiser, K., Dyda, R. Y. & Cerli, C. Molecular trickery in soil organic matter: hidden lignin. Environ. Sci. Technol. 47, 9077–9085 (2013).

    Google Scholar 

  28. Klotzbücher, T., Kalbitz, K., Cerli, C., Hernes, P. J. & Kaiser, K. Gone or just out of sight? The apparent disappearance of aromatic litter components in soils. SOIL 2, 325–335 (2016).

    Google Scholar 

  29. 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).

    Google Scholar 

  30. Lehmann, J. et al. Australian climate–carbon cycle feedback reduced by soil black carbon. Nat. Geosci. 1, 832–835 (2008).

    Google Scholar 

  31. Mikutta, R., Kleber, M., Torn, M. S. & Jahn, R. Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry 77, 25–56 (2006).

    Google Scholar 

  32. Kleber, M. What is recalcitrant soil organic matter? Environ. Chem. 7, 320–332 (2010).

    Google Scholar 

  33. Schmidt, M. W. I. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011).

    Google Scholar 

  34. DiDonato, N., Chen, H., Waggoner, D. & Hatcher, P. G. Potential origin and formation for molecular components of humic acids in soils. Geochim. Cosmochim. Acta 178, 210–222 (2016).

    Google Scholar 

  35. Scatena, F. An Introduction to the Physiography and History of the Bisley Experimental Watersheds in the Luquillo Mountains of Puerto Rico General Technical Report SO-72 (USDA, 1989).

  36. Kleber, M. et al. in Advances in Agronomy Vol. 130 (ed. Sparks, D. L.) Ch. 1 (Elsevier, 2015).

  37. Slessarev, E. W. et al. Water balance creates a threshold in soil pH at the global scale. Nature 540, 567–569 (2016).

    Google Scholar 

  38. Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).

    Google Scholar 

  39. Lundström, U. S., van Breemen, N. & Bain, D. The podzolization process. A review. Geoderma 94, 91–107 (2000).

    Google Scholar 

  40. Kramer, M. G., Sanderman, J., Chadwick, O. A., Chorover, J. & Vitousek, P. M. Long-term carbon storage through retention of dissolved aromatic acids by reactive particles in soil. Glob. Change Biol. 18, 2594–2605 (2012).

    Google Scholar 

  41. Kaiser, K. & Guggenberger, G. The role of DOM sorption to mineral surfaces in the preservation of organic matter in soils. Org. Geochem. 31, 711–725 (2000).

    Google Scholar 

  42. Coward, E. K., Ohno, T. & Plante, A. F. Adsorption and molecular fractionation of dissolved organic matter on iron-bearing mineral matrices of varying crystallinity. Environ. Sci. Technol. 52, 1036–1044 (2018).

    Google Scholar 

  43. Throckmorton, H. M., Bird, J. A., Dane, L., Firestone, M. K. & Horwath, W. R. The source of microbial C has little impact on soil organic matter stabilisation in forest ecosystems. Ecol. Lett. 15, 1257–1265 (2012).

    Google Scholar 

  44. Moorhead, D. L. & Sinsabaugh, R. L. A theoretical model of litter decay and microbial interaction. Ecol. Monogr. 76, 151–174 (2006).

    Google Scholar 

  45. LaRowe, D. E. & Van Cappellen, P. Degradation of natural organic matter: a thermodynamic analysis. Geochim. Cosmochim. Acta 75, 2030–2042 (2011).

    Google Scholar 

  46. Ye, C. et al. Reconciling multiple impacts of nitrogen enrichment on soil carbon: plant, microbial and geochemical controls. Ecol. Lett. 21, 1162–1173 (2018).

    Google Scholar 

  47. Ayres, E., et al. NEON Field and Lab Procedure and Protocol: TIS Soil Pit Sampling Protocol NEON.DOC.001307 (NEON, 2017); https://data.neonscience.org/data-products/DP1.00097.001

  48. Ayres, E. & Durden, D. NEON Field and Lab Procedure and Protocol: TIS Soil Archiving NEON.DOC.000325 (NEON, 2017); https://data.neonscience.org/data-products/DP1.00097.001

  49. Ayres, E. NEON Procedure and Protocol: Producing TIS Soil Archive Subsamples for Users NEON.DOC.001306 (NEON, 2017); https://data.neonscience.org/data-products/DP1.00097.001

  50. Gélinas, Y., Baldock, J. A. & Hedges, J. I. Demineralization of marine and freshwater sediments for CP/MAS 13C NMR analysis. Org. Geochem. 32, 677–693 (2001).

    Google Scholar 

  51. Harbison, G. S. et al. High-resolution carbon-13 NMR of retinal derivatives in the solid state. J. Am. Chem. Soc. 107, 4809–4816 (1985).

    Google Scholar 

  52. Mao, J.-D. et al. Quantitative characterization of humic substances by solid-state carbon-13 nuclear magnetic resonance. Soil Sci. Soc. Am. J. 64, 873–884 (2000).

    Google Scholar 

  53. Longbottom, T. L. & Hockaday, W. C. Molecular and isotopic composition of modern soils derived from kerogen-rich bedrock and implications for the global C cycle. Biogeochemistry 143, 239–255 (2019).

    Google Scholar 

  54. NEON (National Ecological Observatory Network). DP1.00096.001, DP1.10066.001, DP1.10102.001, DP1.10109.001 (accessed September 1, 2019), DP1.10026.001, DP1.10033.001, DP1.10031.001 (accessed May 15, 2020); http://data.neonscience.org

  55. Sullivan, P. F. et al. Climate and species affect fine root production with long-term fertilization in acidic tussock tundra near Toolik Lake, Alaska. Oecologia 153, 643–652 (2007).

    Google Scholar 

  56. SanClements, M. et al. Collaborating with NEON. BioScience 70, 107–107 (2020).

    Google Scholar 

  57. Mu, Q., Zhao, M. & Running, S. W. Improvements to a MODIS global terrestrial evapotranspiration algorithm. Remote Sens. Environ. 115, 1781–1800 (2011).

    Google Scholar 

  58. Revelle, W. psych: Procedures for Personality and Psychological Research v.1.8.12 (Northwestern University, 2018).

  59. Chittleborough, D. J. Indices of weathering for soils and palaeosols formed on silicate rocks. Aust. J. Earth Sci. 38, 115–120 (1991).

    Google Scholar 

  60. Hair, J. F., Risher, J. J., Sarstedt, M. & Ringle, C. M. When to use and how to report the results of PLS-SEM. Eur. Bus. Rev. 31, 2–24 (2019).

    Google Scholar 

  61. Lefcheck, J. S.piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution, and systematics. Methods Ecol. Evol. 7, 573–579 (2016).

    Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the efforts of NEON and NRCS staff in conducting soil sampling and analyses, and E. Ayres for providing access to ‘Megapit’ samples. This research was supported in part by NSF projects DEB 1802745 and EAR 1132124. The National Ecological Observatory Network is a programme sponsored by the National Science Foundation and operated under cooperative agreement by Battelle Memorial Institute.

Author information

Authors and Affiliations

Authors

Contributions

S.J.H., S.R.W. and W.C.H. developed the research concepts, C.Y. and W.C.H. conducted the NMR analyses, S.J.H., C.Y., S.R.W. and W.C.H. analysed data, and S.J.H. and C.Y. wrote the paper with contributions from all authors.

Corresponding authors

Correspondence to Steven J. Hall or William C. Hockaday.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Primary Handling Editor: Tamara Goldin.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Soil sampling locations for this study.

Upper-case letters denote NEON sites and lower-case letters denote other sites as defined in Supplementary Table 1. Map tiles by Stamen Design, under CC BY 3.0. Map data by OpenStreetMap, under ODbL.

Extended Data Fig. 2 Summary boxplots of biogeochemical characteristics of sampled soils or nearby plant material.

Thick lines indicate medians, boxes denote upper and lower quantiles, and whiskers denote samples within 1.5x the interquartile range.

Extended Data Fig. 3 13C CPMAS NMR spectra of all samples following demineralization.

Colors indicate soil order in the US Department of Agriculture soil taxonomy.

Extended Data Fig. 4 Boxplots of SOC functional group fractional abundance as a function of vegetation type (a) and prescribed fire regime (b).

Lignin was significantly greater in forest than grassland/shrubland vegetation (0.23 vs. 0.16, P = 0.011), and protein was significantly greater in grassland/shrubland vegetation than in forest (0.23 vs. 0.15, P = 0.025). Char was significantly greater in sites with prescribed fire than without (0.22 vs. 0.16, P = 0.046). Thick lines indicate medians, boxes denote upper and lower quantiles, and whiskers denote samples within 1.5x the interquartile range.

Extended Data Fig. 5 Correlation heatmap of SOC molecule relative abundance within samples.

The symbols ** and **** indicate corrected P < 0.01 and P < 0.0001, respectively.

Extended Data Fig. 6 Pearson correlations between SOC molecule relative abundance and rotated principal components.

RC1, RC2, and RC3 refer to the rotated principal component axes 1–3.

Extended Data Fig. 7

A description of biogeochemical predictor variables used in this study.

Extended Data Fig. 8 Heatmap of correlations between SOC functional groups and biogeophysical predictors.

The symbols *, **, ***, and **** indicate corrected P < 0.05, P < 0.01, P < 0.001, and P < 0.0001, respectively.

Extended Data Fig. 9 Optimal linear regression models for each rotated principal component (RC) shown in Fig. 2 fit using backwards elimination.

Models are reported for three different datasets/significance criteria: all samples with α = 0.01, all samples with α = 0.05, and all NEON samples with α = 0.05. Model parameter values were calculated using variables standardized by subtracting the mean and dividing by one standard deviation. Values in parentheses are standard errors. Abbreviations for predictors are described in Extended Data Fig. 7.

Supplementary information

Supplementary Information

Supplementary Discussion, Tables 1–7 and Figs. 1–5.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hall, S.J., Ye, C., Weintraub, S.R. et al. Molecular trade-offs in soil organic carbon composition at continental scale. Nat. Geosci. 13, 687–692 (2020). https://doi.org/10.1038/s41561-020-0634-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41561-020-0634-x

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology