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Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments

The ISME Journal volume 10, pages 19391953 (2016) | Download Citation

Abstract

Marine sediments are the largest carbon sink on earth. Nearly half of dark carbon fixation in the oceans occurs in coastal sediments, but the microorganisms responsible are largely unknown. By integrating the 16S rRNA approach, single-cell genomics, metagenomics and transcriptomics with 14C-carbon assimilation experiments, we show that uncultured Gammaproteobacteria account for 70–86% of dark carbon fixation in coastal sediments. First, we surveyed the bacterial 16S rRNA gene diversity of 13 tidal and sublittoral sediments across Europe and Australia to identify ubiquitous core groups of Gammaproteobacteria mainly affiliating with sulfur-oxidizing bacteria. These also accounted for a substantial fraction of the microbial community in anoxic, 490-cm-deep subsurface sediments. We then quantified dark carbon fixation by scintillography of specific microbial populations extracted and flow-sorted from sediments that were short-term incubated with 14C-bicarbonate. We identified three distinct gammaproteobacterial clades covering diversity ranges on family to order level (the Acidiferrobacter, JTB255 and SSr clades) that made up >50% of dark carbon fixation in a tidal sediment. Consistent with these activity measurements, environmental transcripts of sulfur oxidation and carbon fixation genes mainly affiliated with those of sulfur-oxidizing Gammaproteobacteria. The co-localization of key genes of sulfur and hydrogen oxidation pathways and their expression in genomes of uncultured Gammaproteobacteria illustrates an unknown metabolic plasticity for sulfur oxidizers in marine sediments. Given their global distribution and high abundance, we propose that a stable assemblage of metabolically flexible Gammaproteobacteria drives important parts of marine carbon and sulfur cycles.

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Acknowledgements

We greatly acknowledge the crew of R/V Navicula from the ICBM Oldenburg for ship time and assistance. We thank the crew of the R/V Meteor and R/V Sonne and the ROV team of the MARUM Quest 4000 m. We greatly acknowledge the chief scientist Wolfgang Bach for his excellent support during cruise SO216 with R/V Sonne, which was an integral part of the Cluster of Excellence of the MARUM ‘The Ocean in the Earth System, Research Area GB: Geosphere-Biosphere Interactions’ funded by the German Research Foundation (DFG). The cruise SO216 was funded by a grant (03G0216) from the Bundesministerium für Bildung und Forschung (BMBF) awarded to Wolfgang Bach and co-PIs. RS was supported by the US National Science Foundation grant OCE-1232982. We thank Falk Warnecke for support in sediment sampling and for sequencing of the subsurface samples. Special thanks go to Rudolf Amann for helpful discussions and continuous support. This study contributes to the project ABYSS funded by the European Research Council Advanced Investigator Grant 294757 to Antje Boetius. Further funding was provided by the Max Planck Society.

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Affiliations

  1. Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen, Germany

    • Stefan Dyksma
    • , Kerstin Bischof
    • , Bernhard M Fuchs
    • , Dimitri Meier
    • , Anke Meyerdierks
    • , Petra Pjevac
    • , David Probandt
    •  & Marc Mußmann
  2. HGF-MPG Group for Deep Sea Ecology and Technology, Max Planck Institute for Marine Microbiology, Bremen, Germany

    • Katy Hoffmann
  3. Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany

    • Katy Hoffmann
  4. Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria

    • Petra Pjevac
  5. Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Bremen, Germany

    • Michael Richter
  6. Bigelow Laboratory for Ocean Sciences, East Boothbay, USA

    • Ramunas Stepanauskas

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The authors declare no conflict of interest.

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Correspondence to Marc Mußmann.

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https://doi.org/10.1038/ismej.2015.257

Supplementary Information accompanies this paper on The ISME Journal website (http://www.nature.com/ismej)

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