Metabolism in anoxic permeable sediments is dominated by eukaryotic dark fermentation

Abstract

Permeable sediments are common across continental shelves and are critical contributors to marine biogeochemical cycling. Organic matter in permeable sediments is dominated by microalgae, which as eukaryotes have different anaerobic metabolic pathways to bacteria and archaea. Here we present analyses of flow-through reactor experiments showing that dissolved inorganic carbon is produced predominantly as a result of anaerobic eukaryotic metabolic activity. In our experiments, anaerobic production of dissolved inorganic carbon was consistently accompanied by large dissolved H2 production rates, suggesting the presence of fermentation. The production of both dissolved inorganic carbon and H2 persisted following administration of broad spectrum bactericidal antibiotics, but ceased following treatment with metronidazole. Metronidazole inhibits the ferredoxin/hydrogenase pathway of fermentative eukaryotic H2 production, suggesting that pathway as the source of H2 and dissolved inorganic carbon production. Metabolomic analysis showed large increases in lipid production at the onset of anoxia, consistent with documented pathways of anoxic dark fermentation in microalgae. Cell counts revealed a predominance of microalgae in the sediments. H2 production was observed in dark anoxic cultures of diatoms (Fragilariopsis sp.) and a chlorophyte (Pyramimonas) isolated from the study site, substantiating the hypothesis that microalgae undertake fermentation. We conclude that microalgal dark fermentation could be an important energy-conserving pathway in permeable sediments.

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Figure 1: Metabolism measured in FTR experiments.
Figure 2: H2 and metabolite production in permeable sediments.
Figure 3: Conceptual model of benthic algal metabolism in sand sediments.

Change history

  • 14 December 2016

    In the version of this Article originally published, the middle bar in Fig. 1b was mislabelled and should have been labelled NO2-. This has been corrected in all versions of the Article.

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Acknowledgements

This work was supported by the Australian Research Council grant DP1096457 awarded to P.L.M.C. and R.N.G. R.N.G. was additionally supported by Danish Council for Independent Research, Natural Sciences, FNU, (0602-02276B) and the European Research Council through an Advanced Grant (ERC-2010-AdG20100224). The data reported in this paper can be made available by contacting the corresponding authors. We thank J. Middelburg and H. Røy for thoughtful comments on this work.

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All FTR experiments were performed by M.F.B. and supervised by P.L.M.C., who were both jointly responsible for the experimental design and research direction, with significant input from R.N.G. and J.B. Effluent volatile fatty acid analysis was performed by M.F.B. and supervised by P.J.M. Metabolomics analysis was performed by H.H.-S. Algal culture experiments were performed by M.K. and M.F.B. and supervised by J.B. and P.L.M.C. The manuscript was written by M.F.B. and P.L.M.C. All authors contributed to discussion and editing.

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Correspondence to Michael F. Bourke or Perran L. M. Cook.

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Bourke, M., Marriott, P., Glud, R. et al. Metabolism in anoxic permeable sediments is dominated by eukaryotic dark fermentation. Nature Geosci 10, 30–35 (2017). https://doi.org/10.1038/ngeo2843

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