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Mineral protection of soil carbon counteracted by root exudates

Abstract

Multiple lines of existing evidence suggest that climate change enhances root exudation of organic compounds into soils. Recent experimental studies show that increased exudate inputs may cause a net loss of soil carbon. This stimulation of microbial carbon mineralization (‘priming’) is commonly rationalized by the assumption that exudates provide a readily bioavailable supply of energy for the decomposition of native soil carbon (co-metabolism). Here we show that an alternate mechanism can cause carbon loss of equal or greater magnitude. We find that a common root exudate, oxalic acid, promotes carbon loss by liberating organic compounds from protective associations with minerals. By enhancing microbial access to previously mineral-protected compounds, this indirect mechanism accelerated carbon loss more than simply increasing the supply of energetically more favourable substrates. Our results provide insights into the coupled biotic–abiotic mechanisms underlying the ‘priming’ phenomenon and challenge the assumption that mineral-associated carbon is protected from microbial cycling over millennial timescales.

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Figure 1: Proposed mechanisms for the exudate-induced acceleration of the microbial mineralization of native carbon (‘priming effects’) in the rhizosphere.
Figure 2: Exudate effects on artificial rhizosphere soil.
Figure 3: Exudate-induced effects on total soil C and protective mineral phases.
Figure 4: Exudate effect on metal–organic associations in the pore water.

References

  1. Högberg, P. et al. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789–792 (2001).

    Article  Google Scholar 

  2. Clemmensen, K. E. et al. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339, 1615–1618 (2013).

    Article  CAS  Google Scholar 

  3. Phillips, R. P., Finzi, A. C. & Bernhardt, E. S. Enhanced root exudation induces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation. Ecol. Lett. 14, 187–194 (2011).

    Article  Google Scholar 

  4. Carney, K. M., Hungate, B. A., Drake, B. G. & Megonigal, J. P. Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc. Natl Acad. Sci. USA 104, 4990–4995 (2007).

    Article  CAS  Google Scholar 

  5. DeLucia, E. H., Callaway, R. M., Thomas, E. M. & Schlesinger, W. H. Mechanisms of phosphorus acquisition for ponderosa pine seedlings under high CO2 and temperature. Ann. Bot. 79, 111–120 (1997).

    Article  CAS  Google Scholar 

  6. Fransson, P. Elevated CO2 impacts ectomycorrhiza-mediated forest soil carbon flow: Fungal biomass production, respiration and exudation. Fungal Ecol. 5, 85–98 (2012).

    Article  Google Scholar 

  7. Heimann, M. & Reichstein, M. Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451, 289–292 (2008).

    Article  CAS  Google Scholar 

  8. Kuzyakov, Y., Friedel, J. K. & Stahr, K. Review of mechanisms and quantification of priming effects. Soil Biol. Biochem. 32, 1485–1498 (2000).

    Article  CAS  Google Scholar 

  9. Bianchi, T. S. The role of terrestrially derived organic carbon in the coastal ocean: A changing paradigm and the priming effect. Proc. Natl Acad. Sci. USA 108, 19473–19481 (2011).

    Article  CAS  Google Scholar 

  10. Fontaine, S., Mariotti, A. & Abbadie, L. The priming effect of organic matter: A question of microbial competition? Soil Biol. Biochem. 35, 837–843 (2003).

    Article  CAS  Google Scholar 

  11. Horvath, R. S. Microbial co-metabolism and the degradation of organic compounds in nature. Bacteriol. Rev. 36, 146–155 (1972).

    CAS  Google Scholar 

  12. Blagodatskaya, E. & Kuzyakov, Y. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: Critical review. Biol. Fertil. Soils 45, 115–131 (2008).

    Article  Google Scholar 

  13. 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).

    Article  CAS  Google Scholar 

  14. Baisden, W. T., Amundson, R., Cook, A. C. & Brenner, D. L. Turnover and storage of C and N in five density fractions from California annual grassland surface soils. Glob. Biogeochem. Cycles 16, 1117 (2002).

    Google Scholar 

  15. Mikutta, R. et al. Biodegradation of forest floor organic matter bound to minerals via different binding mechanisms. Geochim. Cosmochim. Acta 71, 2569–2590 (2007).

    Article  CAS  Google Scholar 

  16. Chorover, J. & Amistadi, M. K. Reaction of forest floor organic matter at goethite, birnessite and smectite surfaces. Geochim. Cosmochim. Acta 65, 95–109 (2001).

    Article  CAS  Google Scholar 

  17. Conant, R. T. et al. Temperature and soil organic matter decomposition rates—synthesis of current knowledge and a way forward. Glob. Change Biol. 17, 3392–3404 (2011).

    Article  Google Scholar 

  18. 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).

    Article  CAS  Google Scholar 

  19. Rasmussen, C., Southard, R. J. & Horwath, W. R. Soil mineralogy affects conifer forest soil carbon source utilization and microbial priming. Soil Sci. Soc. Am. J. 71, 1141–1150 (2007).

    Article  CAS  Google Scholar 

  20. Kemmitt, S. J. et al. Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass—a new perspective. Soil Biol. Biochem. 40, 61–73 (2008).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  22. Tang, J. Y., Riley, W. J., Koven, C. D. & Subin, Z. M. CLM4-BeTR, a generic biogeochemical transport and reaction module for CLM4: Model development, evaluation, and application. Geosci. Model Dev. 6, 127–140 (2013).

    Article  CAS  Google Scholar 

  23. Jones, D. L., Dennis, P. G. & vanHees, P. A. W. Organic acid behavior in soils—misconceptions and knowledge gaps. Plant Soil 248, 31–41 (2003).

    Article  CAS  Google Scholar 

  24. Neumann, G. & Roemheld, V. The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interface (CRC Press, 2007).

    Google Scholar 

  25. Paterson, E. & Sim, A. Rhizodeposition and C-partitioning of Lolium perenne in axenic culture affected by nitrogen supply and defoliation. Plant Soil 216, 155–164 (1999).

    Article  CAS  Google Scholar 

  26. Phillips, R. P., Erlitz, Y., Bier, R. & Bernhardt, E. S. New approach for capturing soluble root exudates in forest soils. Funct. Ecol. 22, 990–999 (2008).

    Article  Google Scholar 

  27. Brant, J. B., Sulzman, E. W. & Myrold, D. D. Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol. Biochem. 38, 2219–2232 (2006).

    Article  CAS  Google Scholar 

  28. Frey, S. D., Lee, J., Melillo, J. M. & Six, J. The temperature response of soil microbial efficiency and its feedback to climate. Nature Clim. Change 3, 395–398 (2013).

    Article  CAS  Google Scholar 

  29. Schneckenberger, K., Demin, D., Stahr, K. & Kuzyakov, Y. Microbial utilization and mineralization of [14C]glucose added in six orders of concentration to soil. Soil Biol. Biochem. 40, 1981–1988 (2008).

    Article  CAS  Google Scholar 

  30. Fierer, N., Bradford, M. A. & Jackson, R. B. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364 (2007).

    Article  Google Scholar 

  31. Eilers, K. G., Debenport, S., Anderson, S. & Fierer, N. Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol. Biochem. 50, 58–65 (2012).

    Article  CAS  Google Scholar 

  32. Yan, F., Schubert, S. & Mengel, K. Soil pH increase due to biological decarboxylation of organic anions. Soil Biol. Biochem. 28, 617–624 (1996).

    Article  CAS  Google Scholar 

  33. McBride, M. B. Environmental Chemistry of Soils (Oxford Univ. Press, 1994).

    Google Scholar 

  34. Lovley, D. R. Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol. Rev. 55, 259–287 (1991).

    CAS  Google Scholar 

  35. Glinski, J., Stahr, K., Stepniewska, Z. & Brzezinska, M. Changes of redox and pH conditions in a flooded soil amended with glucose and nitrate under laboratory conditions. J. Plant Nutr. Soil Sci. 155, 13–17 (1992).

    CAS  Google Scholar 

  36. Hamer, U. & Marschner, B. Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol. Biochem. 37, 445–454 (2005).

    Article  CAS  Google Scholar 

  37. Falchini, L., Naumova, N., Kuikman, P. J., Bloem, J. & Nannipieri, P. CO2 evolution and denaturing gradient gel electrophoresis profiles of bacterial communities in soil following addition of low molecular weight substrates to simulate root exudation. Soil Biol. Biochem. 35, 775–782 (2003).

    Article  CAS  Google Scholar 

  38. Liu, S. Y. et al. Synchrotron-based mass spectrometry to investigate the molecular properties of mineral–organic associations. Anal. Chem. 85, 6100–6106 (2013).

    Article  CAS  Google Scholar 

  39. Hanley, L. & Zimmermann, R. Light and molecular Ions: The emergence of vacuum UV single-photon ionization in MS. Anal. Chem. 81, 4174–4182 (2009).

    Article  CAS  Google Scholar 

  40. Fischer, H., Ingwersen, J. & Kuzyakov, Y. Microbial uptake of low-molecular-weight organic substances out-competes sorption in soil. Eur. J. Soil Sci. 61, 504–513 (2010).

    Article  CAS  Google Scholar 

  41. Mikutta, R. et al. Biogeochemistry of mineral–organic associations across a long-term mineralogical soil gradient (0.3–4100 kyr), Hawaiian Islands. Geochim. Cosmochim. Acta 73, 2034–2060 (2009).

    Article  CAS  Google Scholar 

  42. 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).

    Article  Google Scholar 

  43. Kunhi Mouvenchery, Y., Kučerík, J., Diehl, D. & Schaumann, G. E. Cation-mediated cross-linking in natural organic matter: A review. Rev. Environ. Sci. Biotechnol. 11, 41–54 (2011).

    Article  Google Scholar 

  44. Fischer, W. R., Flessa, H. & Schaller, G. pH values and redox potentials in microsites of the rhizosphere. Z. Für Pflanzenernähr. Bodenkd. 152, 191–195 (1989).

    Article  CAS  Google Scholar 

  45. Collignon, C., Ranger, J. & Turpault, M. P. Seasonal dynamics of Al- and Fe-bearing secondary minerals in an acid forest soil: Influence of Norway spruce roots (Picea abies (L.) Karst.). Eur. J. Soil Sci. 63, 592–602 (2012).

    Article  CAS  Google Scholar 

  46. Richter, D. D., Markewitz, D., Trumbore, S. E. & Wells, C. G. Rapid accumulation and turnover of soil carbon in a re-establishing forest. Nature 400, 56–58 (1999).

    Article  CAS  Google Scholar 

  47. Wieder, W. R., Grandy, A. S., Kallenbach, C. M. & Bonan, G. B. Integrating microbial physiology and physio-chemical principles in soils with the Microbial-Mineral Carbon Stabilization (MIMICS) model. Biogeosciences 11, 3899–3917 (2014).

    Article  Google Scholar 

  48. Hodge, A. et al. Characterisation and microbial utilisation of exudate material from the rhizosphere of Lolium perenne grown under CO2 enrichment. Soil Biol. Biochem. 30, 1033–1043 (1998).

    Article  CAS  Google Scholar 

  49. Cheng, L. et al. Atmospheric CO2 enrichment facilitates cation release from soil. Ecol. Lett. 13, 284–291 (2010).

    Article  CAS  Google Scholar 

  50. Pérez, D. V., de Campos, R. C. & Novaes, H. B. Soil solution charge balance for defining the speed and time of centrifugation of two Brazilian soils. Commun. Soil Sci. Plant Anal. 33, 2021–2036 (2002).

    Article  Google Scholar 

  51. Kilcoyne, A. L. D. et al. Interferometer-controlled scanning transmission X-ray microscopes at the Advanced Light Source. J. Synchrotron Radiat. 10, 125–136 (2003).

    Article  CAS  Google Scholar 

  52. Smith, R. M. & Martell, A. E. Critical stability constants, enthalpies and entropies for the formation of metal complexes of aminopolycarboxylic acids and carboxylic acids. Sci. Total Environ. 64, 125–147 (1987).

    Article  CAS  Google Scholar 

  53. Højberg, O. & Sørensen, J. Microgradients of microbial oxygen consumption in a barley rhizosphere model system. Appl. Environ. Microbiol. 59, 431–437 (1993).

    Google Scholar 

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Acknowledgements

The authors thank A.L.D. Kilcoyne (ALS beamline 5.3.2.2), S.Y. Liu and M. Ahmed (ALS beamline 9.0.2) for their support. M.Keiluweit was supported by a Lawrence Scholar Fellowship awarded through Lawrence Livermore National Laboratory (LLNL). M.Kleber acknowledges support through Research Agreement No. 2014–1918 with the Institute of Soil Landscape Research, Leibniz-Center for Agricultural Landscape Research (ZALF), Müncheberg, Germany. This work was performed under the auspices of the US Department of Energy by LLNL under Contract DE-AC52-07NA27344. Funding was provided by LLNL LDRD ‘Microbes and Minerals: Imaging C Stabilization’ and a US DOE Genomics Science program award SA-DOE-29318 to J.P-R. The work of P.S.N. is supported by LBNL award No. IC006762 as sub-award from LLNL and DOE-BER Sustainable Systems SFA. The Advanced Light Source is supported by the Director, Office of Science, Office of Basic Energy Sciences, of the US DOE under Contract No. DE-AC02-05CH11231.

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M.Keiluweit performed microcosm set-up, laboratory analyses, synchrotron analyses, data analysis and wrote the manuscript. J.J.B. was responsible for DNA/RNA extractions and data processing. J.J.B. and P.K.W. conducted NanoSIMS analyses. M.Kleber., J.P-R., P.K.W. and P.S.N. supervised the project. All authors discussed the results and contributed to the manuscript.

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Correspondence to Marco Keiluweit.

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Keiluweit, M., Bougoure, J., Nico, P. et al. Mineral protection of soil carbon counteracted by root exudates. Nature Clim Change 5, 588–595 (2015). https://doi.org/10.1038/nclimate2580

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