Metabolism in anoxic permeable sediments is dominated by eukaryotic dark fermentation

Journal name:
Nature Geoscience
Volume:
10,
Pages:
30–35
Year published:
DOI:
doi:10.1038/ngeo2843
Received
Accepted
Published online
Corrected online

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.

At a glance

Figures

  1. Metabolism measured in FTR experiments.
    Figure 1: Metabolism measured in FTR experiments.

    Sediments collected from Port Phillip Bay, Australia (a,c,d) and Kerteminde, Denmark (b). a,b, Oxygen consumption, DIC, nitrite and dinitrogen (as N) production in experiments switched anoxic after O2 consumption was measured, n = 4. c, DIC production rates under oxic and anoxic conditions and in the presence and absence of nitrate, n = 3 for each treatment. d, DIC production under anoxic conditions: control (n = 2), in the presence of 50mgl−1 amoxicillin (n = 2) and 2mmoll−1 HgCl2 (n = 1). All error bars are one standard deviation.

  2. H2 and metabolite production in permeable sediments.
    Figure 2: H2 and metabolite production in permeable sediments.

    Results are shown for FTR experiments (ac) and cultures (d). a, H2 production in the presence and absence of 50μM nitrate. The solid and broken lines represent a change from oxic to anoxic conditions and the addition of 150μmoll−1 ciprofloxacin, respectively, n = 3. b, H2 production in a control and 20mgl−1 metronidazole, n = 3. c, The relative concentration of metabolites during H2 production compared to oxic conditions, n = 3. d, H2 production in cultures of five diatom species and a chlorophyte incubated anoxically in the dark, n = 6. Error bars represent standard deviations.

  3. Conceptual model of benthic algal metabolism in sand sediments.
    Figure 3: Conceptual model of benthic algal metabolism in sand sediments.

    In this energetic environment, ripple migration and sediment resuspension regularly move algal cells many centimetres into the sediment, where it is dark and anoxic. Under these conditions, microalgae undertake dark fermentation associated with high rates of H2 and lipid production25. Enzyme designations are pyruvate ferredoxin oxidoreductase (PFR) and ferredoxin (FDX). Lightly shaded areas represent declining oxygen concentration within the sediment. Yellow shaded area represents anoxic permeable sediment.

Change history

Corrected online 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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Author information

Affiliations

  1. Water Studies Centre, School of Chemistry, Monash University, Wellington Road, Clayton, Victoria 3800, Australia

    • Michael F. Bourke &
    • Perran L. M. Cook
  2. Australian Centre for Research on Separation Science, School of Chemistry, Monash University, Wellington Road, Clayton, Victoria 3800, Australia

    • Philip J. Marriott
  3. University of Southern Denmark, Nordic Centre for Earth Evolution, Odense M-5230, Denmark

    • Ronnie N. Glud &
    • Harald Hasler-Sheetal
  4. Scottish Association for Marine Science, Oban PA37 1QA, UK

    • Ronnie N. Glud
  5. University of Aarhus, Arctic Research Centre, Aarhus DK-8000, Denmark

    • Ronnie N. Glud
  6. University of Southern Denmark, Villum Center for Bioanalytical Sciences, Odense M-5230, Denmark

    • Harald Hasler-Sheetal
  7. Department of Marine Biology, Texas A&M University, Galveston, Texas 77554, USA

    • Manoj Kamalanathan
  8. School of Biological Sciences, Monash University, Clayton, Victoria 3800, Australia

    • John Beardall &
    • Chris Greening

Contributions

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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The authors declare no competing financial interests.

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