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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.

Soil carbon (C) stabilization has become an important topic in recent years owing to changes in global climate and atmospheric chemistry1,2. Globally, soil contains a large amount of C—twice that in the atmosphere and more than the C in vegetation and the atmosphere combined3–5. Owing to its large size, small changes in the balance between inputs to and outputs from the soil C pool would have a significant impact on atmospheric CO2, and could either reduce or exacerbate the consequences of burning fossil fuels6–8. Because soil C cycling is ultimately the consequence of microbial growth and activity, understanding organic matter decomposition, transformation and sequestration in soils demands improved knowledge of how microbial physiology regulates the processes controlling biogeochemical cycling, climate change and ecosystem sustainability9,10.

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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.

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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.

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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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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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