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Evidence for complete denitrification in a benthic foraminifer

Nature volume 443, pages 93–96 (2006)Cite this article

Abstract

Benthic foraminifera are unicellular eukaryotes found abundantly in many types of marine sediments. Many species survive and possibly reproduce in anoxic habitats1, but sustainable anaerobic metabolism has not been previously described. Here we demonstrate that the foraminifer Globobulimina pseudospinescens accumulates intracellular nitrate stores and that these can be respired to dinitrogen gas. The amounts of nitrate detected are estimated to be sufficient to support respiration for over a month. In a Swedish fjord sediment where G. pseudospinescens is the dominant foraminifer, the intracellular nitrate pool in this species accounted for 20% of the large, cell-bound, nitrate pool present in an oxygen-free zone. Similarly high nitrate concentrations were also detected in foraminifera Nonionella cf. stella and a Stainforthia species, the two dominant benthic taxa occurring within the oxygen minimum zone of the continental shelf off Chile. Given the high abundance of foraminifera in anoxic marine environments1,2,3, these new findings suggest that foraminifera may play an important role in global nitrogen cycling and indicate that our understanding of the complexity of the marine nitrogen cycle is far from complete.

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Figure 1: Foraminifera, oxygen and nitrate in sediment.
Figure 2: SEM and TEM micrographs of the investigated foraminifer species.
Figure 3: N2 production in G. pseudospinescens.

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Acknowledgements

We thank P. Engström, J. Brandsma, V. A. Gallardo, B. B. Jørgensen, E. Frandsen, G. Ittman, S. Petersen, K. L. Knudsen, G. J. Janssen, P. Sørensen and L. Pierson for their support. The work was supported by the Carlsberg Foundation, Denmark (N.R.-P.); the National Science Research Foundation, Denmark (N.R.-P., T.C. and N.P.R.); the Netherlands Organization for Scientific Research (NWO-ALW biogeosphere; G.J.v.d.Z. and M.S.M.J.) and the Swedish Research Council (S.P.E.). Author Contributions A.M.L., M.C.S., N.R.-P., S.I., L.P.N. and N.P.R. performed the sampling. A.M.L, G.J.v.d.Z and T.C. carried out the foraminifer identification. N.R.-P., N.P.R., E.P.-O., S.I., L.P.N. and A.M.L. performed the nitrate and denitrification rate measurements; J.W.M.D., H.J.M.O.d.C., T.C. and M.C.S. performed the microscopy. The research was conceived by N.R.-P., S.P.E., G.J.v.d.Z., M.S.M.J., H.J.M.O.d.C., A.M.L., N.P.R, L.P.N. and S.I. All authors contributed to interpreting the data and writing the paper.

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Authors and Affiliations

  1. Department of Marine Ecology, National Environmental Research Institute, Vejlsøvej 25, DK-8600, Silkeborg, Denmark

    Nils Risgaard-Petersen

  2. Department of Earth Sciences, Utrecht University, Faculty of Geosciences, Budapestlaan 4, NL-3584 CD, Utrecht, The Netherlands

    Alexandra M. Langezaal & Gijsbert J. van der Zwaan

  3. Department of Biological Sciences, University of Aarhus, Ny Munkegade, Building 1540, DK-8000, Aarhus C, Denmark

    Signe Ingvardsen, Lars Peter Nielsen, Niels Peter Revsbech & Tomas Cedhagen

  4. Department of Microbiology,

    Markus C. Schmid, Mike S. M. Jetten & Huub J. M. Op den Camp

  5. Department of Plant Cell Biology, IWWR, Radboud University Nijmegen, Toernooiveld 1, NL-6525 ED, Nijmegen, The Netherlands

    Jan W. M. Derksen

  6. Department of Aquatic Ecology (CSIC), Centre of Environmental Sciences, Serrano 115 dpdo., E-28006, Madrid, Spain

    Elisa Piña-Ochoa

  7. Department of Marine Ecology, Kristineberg Marine Research Station, Göteborg University, S-450 34, Fiskebäckskil, Sweden

    Susanne P. Eriksson

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  1. Nils Risgaard-Petersen
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Correspondence to Nils Risgaard-Petersen.

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Supplementary information

Supplementary Methods

This file contains methodology used for measuring denitrification in a foraminifer and the procedure used for calculation of the denitrification activity for a bacterial cell. There is also one figure. (PDF 59 kb)

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Risgaard-Petersen, N., Langezaal, A., Ingvardsen, S. et al. Evidence for complete denitrification in a benthic foraminifer. Nature 443, 93–96 (2006). https://doi.org/10.1038/nature05070

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