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The importance of anabolism in microbial control over soil carbon storage

Nature Microbiology volume 2, Article number: 17105 (2017) Cite this article

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Studies of the decomposition, transformation and stabilization of soil organic matter (SOM) have dramatically increased in recent years owing to growing interest in studying the global carbon (C) cycle as it pertains to climate change. While it is readily accepted that the magnitude of the organic C reservoir in soils depends upon microbial involvement, as soil C dynamics are ultimately the consequence of microbial growth and activity, it remains largely unknown how these microorganism-mediated processes lead to soil C stabilization. Here, we define two pathways—ex vivo modification and in vivo turnover—which jointly explain soil C dynamics driven by microbial catabolism and/or anabolism. Accordingly, we use the conceptual framework of the soil ‘microbial carbon pump’ (MCP) to demonstrate how microorganisms are an active player in soil C storage. The MCP couples microbial production of a set of organic compounds to their further stabilization, which we define as the entombing effect. This integration captures the cumulative long-term legacy of microbial assimilation on SOM formation, with mechanisms (whether via physical protection or a lack of activation energy due to chemical composition) that ultimately enable the entombment of microbial-derived C in soils. We propose a need for increased efforts and seek to inspire new studies that utilize the soil MCP as a conceptual guideline for improving mechanistic understandings of the contributions of soil C dynamics to the responses of the terrestrial C cycle under global change.

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Figure 1: Schematic diagram of microbial metabolic processes involved in C cycling in terrestrial ecosystems.
Figure 2: Priming effect versus entombing effect regulates fluctuation of the stable soil C pool.
Figure 3: Ex vivo modification versus in vivo turnover of microbial metabolic processes controls the chemical fate of soil C.

References

  1. Lal, R. Soil carbon sequestration impacts on global climate change and food security. Science 304, 1623–1627 (2004).

    Article  CAS  Google Scholar 

  2. Trumbore, S. E. Potential responses of soil organic carbon to global environmental change. Proc. Natl Acad. Sci. USA 94, 8284–8291 (1997).

    Article  CAS  Google Scholar 

  3. Eswaran, H., Van Den Berg, E. & Reich, P. Organic carbon in soils of the world. Soil Sci. Soc. Am. J. 57, 192–194 (1993).

    Article  Google Scholar 

  4. Balser, T. C. in Encyclopedia of Soils in the Environment (ed. Hillel, D. ) 195–207 (Elsevier, 2005).

    Book  Google Scholar 

  5. Stockmann, U. et al. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agr. Ecosyst. Environ. 164, 80–99 (2013).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Rustad, L. E., Huntington, T. G. & Boone, R. D. Controls on soil respiration: implications for climate change. Biogeochemistry 48, 1–6 (2000).

    Article  Google Scholar 

  8. Liang, C. & Balser, T. C. Warming and nitrogen deposition lessen microbial residue contribution to soil carbon pool. Nat. Commun. 3, 1222 (2012).

  9. Bardgett, R. D., Freeman, C. & Ostle, N. J. Microbial contributions to climate change through carbon cycle feedbacks. ISME J. 2, 805–814 (2008).

    Article  CAS  Google Scholar 

  10. Schimel, J. & Schaeffer, S. M. Microbial control over carbon cycling in soil. Front. Microbiol. 3, 1–11 (2012).

    Article  Google Scholar 

  11. Liang, C. & Balser, T. C. Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat. Rev. Microbiol. 9, 75 (2011).

  12. 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).

    Article  Google Scholar 

  13. Benner, R. Biosequestration of carbon by heterotrophic microorganisms. Nat. Rev. Microbiol. 9, 75–75 (2011).

    Article  CAS  Google Scholar 

  14. Miltner, A., Bombach, P., Schmidt-Brücken, B. & Kästner, M. SOM genesis: microbial biomass as a significant source. Biogeochemistry 111, 41–55 (2012).

    Article  CAS  Google Scholar 

  15. Schaeffer, A., Nannipieri, P., Kästner, M., Schmidt, B. & Botterweck, J. From humic substances to soil organic matter–microbial contributions. In honour of Konrad Haider and James P. Martin for their outstanding research contribution to soil science. J. Soils Sediments 15, 1865–1881 (2015).

    Article  Google Scholar 

  16. Ludwig, M. et al. Microbial contribution to SOM quantity and quality in density fractions of temperate arable soils. Soil Biol. Biochem. 81, 311–322 (2015).

    Article  CAS  Google Scholar 

  17. Kindler, R., Miltner, A., Richnow, H.-H. & Kastner, M. Fate of gram-negative bacterial biomass in soil—mineralization and contribution to SOM. Soil Biol. Biochem. 38, 2860–2870 (2006).

    Article  CAS  Google Scholar 

  18. Schweigert, M., Herrmann, S., Miltner, A., Fester, T. & Kästner, M. Fate of ectomycorrhizal fungal biomass in a soil bioreactor system and its contribution to soil organic matter formation. Soil Biol. Biochem. 88, 120–127 (2015).

    Article  CAS  Google Scholar 

  19. Liang, C., Cheng, G., Wixon, D. & Balser, T. An absorbing Markov chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry 106, 303–309 (2011).

    Article  Google Scholar 

  20. Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: Long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599 (2010).

    Article  CAS  Google Scholar 

  21. Kögel-Knabner, I. & Amelung, W. in Treatise on Geochemistry 2nd edn (eds. Holland, H. & Turekian, K. ) 157–215 (Elsevier, 2014).

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  23. Hayes, M. H. B. & Swift, R. S. An appreciation of the contribution of Frank Stevenson to the advancement of studies of soil organic matter and humic substances. J. Soils Sediments http://dx.doi.org/10.1007/s11368-016-1636-6 (2017).

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

    Article  CAS  Google Scholar 

  25. Lehmann, J. et al. Spatial complexity of soil organic matter forms at nanometre scales. Nat. Geosci. 1, 238–242 (2008).

    Article  CAS  Google Scholar 

  26. Oades, J. M. The retention of organic matter in soils. Biogeochemistry 5, 35–70 (1988).

    Article  CAS  Google Scholar 

  27. Hedges, J. I. & Oades, J. M. Comparative organic geochemistries of soils and marine sediments. Org. Geochem. 27, 319–361 (1997).

    Article  CAS  Google Scholar 

  28. Sollins, P. et al. Sequential density fractionation across soils of contrasting mineralogy: evidence for both microbial- and mineral-controlled soil organic matter stabilization. Biogeochemistry 96, 209–231 (2009).

    Article  CAS  Google Scholar 

  29. 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. Tot. Environ. 404, 297–307 (2008).

    Article  CAS  Google Scholar 

  30. Hagerty, S. B. et al. Accelerated microbial turnover but constant growth efficiency with warming in soil. Nat. Clim. Change 4, 903–906 (2014).

    Article  CAS  Google Scholar 

  31. Cornwell, W. K. et al. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol. Lett. 11, 1065–1071 (2008).

    Article  Google Scholar 

  32. Waldrop, M. P. & Firestone, M. K. Microbial community utilization of recalcitrant and simple carbon compounds: Impact of oak-woodland plant communities. Oecologia 138, 275–284 (2004).

    Article  Google Scholar 

  33. Strickland, M. S., Lauber, C., Fierer, N. & Bradford, M. A. Testing the functional significance of microbial community composition. Ecology 90, 441–451 (2009).

    Article  Google Scholar 

  34. Poll, C., Ingwersen, J., Stemmer, M., Gerzabek, M. H. & Kandeler, E. Mechanisms of solute transport affect small-scale abundance and function of soil microorganisms in the detritusphere. Eur. J. Soil Sci. 57, 583–595 (2006).

    Article  Google Scholar 

  35. Schimel, J., Balser, T. C. & Wallenstein, M. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386–1394 (2007).

    Article  Google Scholar 

  36. Strickland, M. S. & Rousk, J. Considering fungal:bacterial dominance in soils – methods, controls, and ecosystem implications. Soil Biol. Biochem. 42, 1385–1395 (2010).

    Article  CAS  Google Scholar 

  37. Liang, C., Fujinuma, R., Wei, L. & Balser, T. C. Tree species-specific effects on soil microbial residues in an upper Michigan old-growth forest system. Forestry 80, 65–72 (2007).

    Article  Google Scholar 

  38. Zhang, X. et al. Land-use effects on amino sugars in particle size fractions of an Argiudoll. Appl. Soil Ecol. 11, 271–275 (1999).

    Article  Google Scholar 

  39. Nakas, J. P. & Klein, D. A. Decomposition of microbial cell components in a semi-arid grassland soil. Appl. Environ. Microbiol. 38, 454–460 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Six, J., Frey, S. D., Thiet, R. K. & Batten, K. M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 70, 555–569 (2006).

    Article  CAS  Google Scholar 

  41. Wardle, D. A. A comparative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol. Rev. 67, 321–358 (1992).

    Article  Google Scholar 

  42. Dalal, R. C. Soil microbial biomass: what do the numbers really mean? Aust. J. Exp. Agr. 38, 649–665 (1998).

    Article  Google Scholar 

  43. Xu, X., Thornton, P. E. & Post, W. M. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob. Ecol. Biogeogr. 22, 737–749 (2013).

    Article  Google Scholar 

  44. Potthoff, M., Dyckmans, J., Flessa, H., Beese, F. & Joergensen, R. Decomposition of maize residues after manipulation of colonization and its contribution to the soil microbial biomass. Biol. Fertil. Soils 44, 891–895 (2008).

    Article  CAS  Google Scholar 

  45. von Lützow, M. et al. Stabilization of organic matter in temperate soils: Mechanisms and their relevance under different soil conditions – a review. Eur. J. Soil Sci. 57, 426–445 (2006).

    Article  Google Scholar 

  46. Sollins, P., Homann, P. & Caldwell, B. A. Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74, 65–105 (1996).

    Article  Google Scholar 

  47. Lehmann, J., Kinyangi, J. & Solomon, D. Organic matter stabilization in soil microaggregates: implications from spatial heterogeneity of organic carbon contents and carbon forms. Biogeochemistry 85, 45–57 (2007).

    Article  Google Scholar 

  48. Wan, J., Tyliszczak, T. & Tokunaga, T. K. Organic carbon distribution, speciation, and elemental correlations within soil microaggregates: applications of STXM and NEXAFS spectroscopy. Geochim. Cosmochim. Acta 71, 5439–5449 (2007).

    Article  CAS  Google Scholar 

  49. Solomon, D. et al. Micro- and nano-environments of carbon sequestration: multi-element STXM–NEXAFS spectromicroscopy assessment of microbial carbon and mineral associations. Chem. Geol. 329, 53–73 (2012).

    Article  CAS  Google Scholar 

  50. Chen, C., Dynes, J. J., Wang, J., Karunakaran, C. & Sparks, D. L. Soft X-ray spectromicroscopy study of mineral-organic matter associations in pasture soil clay fractions. Environ. Sci. Technol. 48, 6678–6686 (2014).

    Article  CAS  Google Scholar 

  51. 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).

  52. Lechtenfeld, O. J., Hertkorn, N., Shen, Y., Witt, M. & Benner, R. Marine sequestration of carbon in bacterial metabolites. Nat. Commun. 6, 6711 (2015).

  53. Cui, L. et al. Impacts of vegetation type and climatic zone on neutral sugar distribution in natural forest soils. Geoderma 282, 139–146 (2016).

    Article  CAS  Google Scholar 

  54. Zhu, B. & Cheng, W. Rhizosphere priming effect increases the temperature sensitivity of soil organic matter decomposition. Glob. Change Biol. 17, 2172–2183 (2011).

    Article  Google Scholar 

  55. Nottingham, A. T., Griffiths, H., Chamberlain, P. M., Stott, A. W. & Tanner, E. V. J. Soil priming by sugar and leaf-litter substrates: a link to microbial groups. Appl. Soil. Ecol. 42, 183–190 (2009).

    Article  Google Scholar 

  56. Fan, Z. & Liang, C. Significance of microbial asynchronous anabolism to soil carbon dynamics driven by litter inputs. Sci. Rep. 5, 9575 (2015).

  57. Wallenstein, M. D. et al. Litter chemistry changes more rapidly when decomposed at home but converges during decomposition–transformation. Soil. Biol. Biochem. 57, 311–319 (2013).

    Article  CAS  Google Scholar 

  58. Angers, D. A. & Mehuys, G. R. Barley and alfalfa cropping effects on carbohydrate contents of a clay soil and its size fractions. Soil. Biol. Biochem. 22, 285–288 (1990).

    Article  CAS  Google Scholar 

  59. Quideau, S. A., Chadwick, O. A., Benesi, A., Graham, R. C. & Anderson, M. A. A direct link between forest vegetation type and soil organic matter composition. Geoderma 104, 41–60 (2001).

    Article  CAS  Google Scholar 

  60. Stewart, C. E., Neff, J. C., Amatangelo, K. L. & Vitousek, P. M. Vegetation effects on soil organic matter chemistry of aggregate fractions in a Hawaiian forest. Ecosystems 14, 382–397 (2011).

    Article  CAS  Google Scholar 

  61. Filley, T. R., Boutton, T. W., Liao, J. D., Jastrow, J. D. & Gamblin, D. E. Chemical changes to nonaggregated particulate soil organic matter following grassland-to-woodland transition in a subtropical savanna. J. Geophys. Res. Biogeosci. 113, 10269–10269 (2008).

    Google Scholar 

  62. Wickings, K., Grandy, A. S., Reed, S. C. & Cleveland, C. C. The origin of litter chemical complexity during decomposition. Ecol. Lett. 15, 1180–1188 (2012).

    Article  Google Scholar 

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Acknowledgements

We would like to thank X. Zhang, T. Balser, J. Tiedje, E. DeLucia, J. Kao-Kniffin and M. Kästner for their help with the evolution of ideas and concepts, along with the career development of C.L. We would like to thank K. Wickings and H. Gan for valuable inputs during preparation of the manuscript, and J. Lehmann for constructive comments and suggestions to improve the manuscript at a later stage. Particularly, we would like to thank X. Zhu for enhancing the visual quality of the figures. This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDB15010303), the National Natural Science Foundation of China (No. 41471218), the National Key Research and Development Program of China (No. 2016YFA0600802), and the US Department of Energy, Office of Science, Office of Biological and Environmental Research. The grants or other support to C.L. from the National Thousand Young Talents Program of China and the Alexander von Humboldt Foundation of Germany are also acknowledged with gratitude.

Author information

Authors and Affiliations

  1. Key laboratory of Forest Ecology and Management, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, 110016, China

    Chao Liang

  2. Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, 93106, California, USA

    Joshua P. Schimel

  3. Environmental Science Division, Argonne National Laboratory, Argonne, 60439, Illinois, USA

    Julie D. Jastrow

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  1. Chao Liang
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  2. Joshua P. Schimel
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  3. Julie D. Jastrow
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C.L. conceived the ideas, developed the conceptual framework, and drafted the original manuscript. C.L., J.P.S. and J.D.J. contributed to concept polishing and critical revision of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Chao Liang.

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Liang, C., Schimel, J. & Jastrow, J. The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2, 17105 (2017). https://doi.org/10.1038/nmicrobiol.2017.105

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