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Altered carbon turnover processes and microbiomes in soils under long-term extremely high CO2 exposure

Nature Microbiology volume 1, Article number: 15025 (2016) Cite this article

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A Corrigendum to this article was published on 11 February 2016

Abstract

There is only limited understanding of the impact of high p(CO2) on soil biomes. We have studied a floodplain wetland where long-term emanations of temperate volcanic CO2 (mofettes) are associated with accumulation of carbon from the Earth's mantle. With an integrated approach using isotope geochemistry, soil activity measurements and multi-omics analyses, we demonstrate that high (nearly pure) CO2 concentrations have strongly affected pathways of carbon production and decomposition and therefore carbon turnover. In particular, a promotion of dark CO2 fixation significantly increased the input of geogenic carbon in the mofette when compared to a reference wetland soil exposed to normal levels of CO2. Radiocarbon analysis revealed that high quantities of mofette soil carbon originated from the assimilation of geogenic CO2 (up to 67%) via plant primary production and subsurface CO2 fixation. However, the preservation and accumulation of almost undegraded organic material appeared to be facilitated by the permanent exclusion of meso- to macroscopic eukaryotes and associated physical and/or ecological traits rather than an impaired biochemical potential for soil organic matter decomposition. Our study shows how CO2-induced changes in diversity and functions of the soil community can foster an unusual biogeochemical profile.

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Figure 1: Bulk soil geochemistry of mofette and reference.
Figure 2: Frequency profiles of transcripts with annotations of CAZY classes in mofette (Mof.) and reference (Ref.) metatranscriptomes.
Figure 3: Conceptual model summarizing the effects of extremely high CO2 concentration on major wetland floodplain soil enzymatic functions and soil food web diversity, as deduced from metatranscriptomes and metagenomes.
Figure 4: Rates of CO2 fixation and formation in mofette and reference soil incubations.

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Acknowledgements

The authors thank H. Pfanz for motivation to work on the studied mofettes, K. Henkel for assistance during thermogravimetric analysis, J. Wendt and H. Geilmann for assistance with TOC and δ13C-TOC analysis, A. Hädrich, D. Akob, C. Simon, J. Kuhr and S. Vetter for help during sampling, and S. Kolb for discussions. Sequencing was performed by the Norwegian Sequencing Centre (www.sequencing.uio.no), a national technology platform supported by the Functional Genomics and Infrastructure programmes of the Research Council of Norway and the Southeastern Regional Health Authorities. This work was funded by the Deutsche Forschungsgemeinschaft through grant KU1367/10-1, the graduate research training group ‘Alternation and element mobility at the microbe–mineral interface’ (GRK 1257) and the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig.

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Authors and Affiliations

  1. Aquatic Geomicrobiology, Institute of Ecology, Friedrich Schiller University Jena, Dornburger Str. 159, D-07743 Jena, Germany

    Felix Beulig & Kirsten Küsel

  2. Division of Archaea Biology and Ecogenomics, Department of Ecogenomics and Systems Biology, University of Vienna, Althanstraße 14, 1090 Vienna, Austria

    Tim Urich

  3. Bacterial Physiology, Institute for Microbiology, Ernst Moritz Arndt University Greifswald, Friedrich-Ludwig-Jahnstr. 15, 17489 Greifswald, Germany

    Tim Urich

  4. Max Planck Institute for Biogeochemistry, POB 100164 10, 07701 Jena, Germany

    Martin Nowak, Susan E. Trumbore & Gerd Gleixner

  5. Medical Genetics, Oslo University Hospital and University of Oslo, Kirkeveien 166, 0407 Oslo, Norway

    Gregor D. Gilfillan & Kristine E. Fjelland

  6. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, D-04103 Leipzig, Germany

    Kirsten Küsel

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Contributions

F.B. conceived, designed and performed the experiments, analysed the data and wrote the main paper. T.U. helped to design and analyse metatranscriptome and -genome sequencing experiments. M.N. performed radiocarbon measurements of soil and plant material and helped with 13C bulk soil measurements. S.E.T. and G.G. contributed to data discussion and structuring of the manuscript. G.D.G. and K.E.F. performed the metatranscriptome and -genome sequencing. F.B., K.K., S.E.T. and G.G. contributed to data discussion and structuring of the manuscript. All co-authors commented on and provided edits to the manuscript.

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Correspondence to Kirsten Küsel.

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The authors declare no competing financial interests.

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Beulig, F., Urich, T., Nowak, M. et al. Altered carbon turnover processes and microbiomes in soils under long-term extremely high CO2 exposure. Nat Microbiol 1, 15025 (2016). https://doi.org/10.1038/nmicrobiol.2015.25

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