Evidence for complete denitrification in a benthic foraminifer (original) (raw)

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.

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Figure 2: SEM and TEM micrographs of the investigated foraminifer species.

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Figure 3: N 2 production in G. pseudospinescens.

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References

  1. Bernhard, J. M. Microaerophilic and facultative anaerobic benthic foraminifera: a review of experimental and ultrastructural evidence. Rev. de Paléobiol 15, 261–275 (1996)
    Google Scholar
  2. Gooday, A. J., Bernhard, J. M., Levin, L. A. & Suhr, S. B. Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-sea Res. II 47, 25–54 (2000)
    Article ADS Google Scholar
  3. Levin, L. et al. Benthic processes on the Peru margin: a transect across the oxygen minimum zone during the 1997–98 El Nino. Prog. Oceanogr. 53, 1–27 (2002)
    Article ADS Google Scholar
  4. Fontanier, C. et al. Seasonal and interannual variability of benthic foraminiferal faunas at 550 m depth in the Bay of Biscay. Deep-sea Res. I 50, 457–494 (2003)
    Article Google Scholar
  5. Alberts, B., et al. Molecular Biology of the Cell (Garland Science, New York, 2002)
    Google Scholar
  6. Bernhard, J. M. & Reimers, C. E. Benthic foraminiferal population fluctuations related to anoxia: Santa Barbara Basin. Biogeochemistry 15, 127–149 (1991)
    Article CAS Google Scholar
  7. Dalsgaard, T., Canfield, D. E., Petersen, J., Thamdrup, B. & Acuña-González, J. N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422, 606–608 (2003)
    Article ADS CAS Google Scholar
  8. Chen, F., Xia, Q. & Ju, L. K. Aerobic denitrification of Pseudomonas aeruginosa monitored by online NAD(P)H fluorescence. Appl. Environ. Microbiol. 69, 6715–6722 (2003)
    Article CAS PubMed PubMed Central Google Scholar
  9. Finlay, B. J., Span, A. S. W. & Harman, J. M. P. Nitrate respiration in primitive eukaryotes. Nature 303, 333–336 (1983)
    Article ADS CAS Google Scholar
  10. Tielens, A. G. M., Rotte, C., van Hellemond, J. J. & Martin, W. Mitochondria as we don't know them. Trends Biochem. Sci. 27, 564–572 (2002)
    Article CAS Google Scholar
  11. Geslin, E., Heinz, P., Jorissen, F. & Hemleben, C. Migratory responses of deep-sea benthic foraminifera to variable oxygen conditions: laboratory investigations. Mar. Micropaleontol. 53, 227–243 (2004)
    Article ADS Google Scholar
  12. Zopfi, J., Kjaer, T., Nielsen, L. P. & Jorgensen, B. B. Ecology of Thioploca spp.: nitrate and sulfur storage in relation to chemical microgradients and influence of Thioploca spp. on the sedimentary nitrogen cycle. Appl. Environ. Microbiol. 67, 5530–5537 (2001)
    Article CAS PubMed PubMed Central Google Scholar
  13. Engström, P., Dalsgaard, T., Hulth, S. & Aller, R. C. Anaerobic ammonium oxidation by nitrite (anammox): Implications for N2 production in coastal marine sediments. Geochim. Cosmochim. Acta 69, 2057–2065 (2005)
    Article ADS Google Scholar
  14. Huettel, M., Forster, S., Klöser, S. & Fossing, H. Vertical migration in the sediment-dwelling sulfur bacteria Thioploca spp. in overcoming diffusion limitations. Appl. Environ. Microbiol. 62, 1863–1872 (1996)
    CAS PubMed PubMed Central Google Scholar
  15. Larsen, L. H., Kjaer, T. & Revsbech, N. P. A microscale NO-3 biosensor for environmental applications. Anal. Chem. 69, 3527–3531 (1997)
    Article CAS PubMed Google Scholar
  16. Revsbech, N. P. An oxygen microelectrode with a guard cathode. Limnol. Oceanogr. 34, 474–478 (1989)
    Article ADS CAS Google Scholar
  17. Meyer, R. L., Kjaer, T. & Revsbech, N. P. Use of NOx- microsensors to estimate the activity of sediment nitrification and NOx- consumption along an estuarine salinity, nitrate, and light gradient. Aquat. Microb. Ecol. 26, 181–193 (2001)
    Article Google Scholar
  18. Sayama, M. Presence of nitrate-accumulating sulfur bacteria and their influence on nitrogen cycling in a shallow coastal marine sediment. Appl. Environ. Microbiol. 67, 3481–3487 (2001)
    Article CAS PubMed PubMed Central Google Scholar
  19. Braman, R. S. & Hendrix, S. A. Nanogram nitrite and nitrate determination in environmental and biological-materials by vanadium(III) reduction with chemi-luminescence detection. Anal. Chem. 61, 2715–2718 (1989)
    Article CAS PubMed Google Scholar
  20. Kuypers, M. M. M. et al. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611 (2003)
    Article ADS CAS Google Scholar
  21. Raghoebarsing, A. A. et al. Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436, 1153–1156 (2005)
    Article ADS CAS Google Scholar
  22. Risgaard-Petersen, N. & Rysgaard, S. in Methods in Applied Soil Microbiology and Biochemistry (eds Alef, K. & Nannipieri, P.) 287–296 (Academic, London, 1995)
    Google Scholar
  23. Risgaard-Petersen, N., Rysgaard, S. & Revsbech, N. P. A sensitive assay for determination of 14N/15N isotope distribution in NO3-. J. Microbiol. Meth. 17, 155–164 (1993)
    Article CAS Google Scholar
  24. Vester, F. & Ingvorsen, K. Improved most-probable-number method to detect sulfate-reducing bacteria with natural media and a radiotracer. Appl. Environ. Microbiol. 64, 1700–1707 (1998)
    CAS PubMed PubMed Central Google Scholar
  25. Bernhard, J. M. Distinguishing live from dead foraminifera: methods review and proper applications. Micropaleontology 46, 38–46 (2000)
    Google Scholar
  26. Nielsen, L. P. Denitrification in sediments determined from nitrogen isotope pairing. FEMS Microbiol. Ecol. 86, 357–362 (1992)
    Article CAS Google Scholar

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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

Authors

  1. Nils Risgaard-Petersen
  2. Alexandra M. Langezaal
  3. Signe Ingvardsen
  4. Markus C. Schmid
  5. Mike S. M. Jetten
  6. Huub J. M. Op den Camp
  7. Jan W. M. Derksen
  8. Elisa Piña-Ochoa
  9. Susanne P. Eriksson
  10. Lars Peter Nielsen
  11. Niels Peter Revsbech
  12. Tomas Cedhagen
  13. Gijsbert J. van der Zwaan

Corresponding author

Correspondence toNils Risgaard-Petersen.

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Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Methods (download PDF )

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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Editorial Summary

Living without oxygen

Several foraminiferal protozoa species grow in anoxic zones in marine sediment, but the type of anaerobic respiration that sustains them was not known. These organisms have now been found to accumulate nitrate intracellularly at concentrations more than 500 times the environmental values. The nitrate substitutes for oxygen in these anoxic habitats. The large amounts of nitrate that accumulate may even allow them to 'hold their breath' for more than a month.