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Research Article

Diatoms respire nitrate to survive dark and anoxic conditions

Anja Kamp, Dirk de Beer, Jana L. Nitsch, Gaute Lavik, and Peter Stief
  1. Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany

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PNAS first published March 14, 2011; https://doi.org/10.1073/pnas.1015744108
Anja Kamp
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  • For correspondence: akamp@mpi-bremen.de
Dirk de Beer
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Jana L. Nitsch
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Gaute Lavik
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Peter Stief
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  1. Edited by James M. Tiedje, Center for Microbial Ecology, East Lansing, MI, and approved February 23, 2011 (received for review October 20, 2010)

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Abstract

Diatoms survive in dark, anoxic sediment layers for months to decades. Our investigation reveals a correlation between the dark survival potential of marine diatoms and their ability to accumulate NO3− intracellularly. Axenic strains of benthic and pelagic diatoms that stored 11–274 mM NO3− in their cells survived for 6–28 wk. After sudden shifts to dark, anoxic conditions, the benthic diatom Amphora coffeaeformis consumed 84–87% of its intracellular NO3− pool within 1 d. A stable-isotope labeling experiment proved that 15NO3− consumption was accompanied by the production and release of 15NH4+, indicating dissimilatory nitrate reduction to ammonium (DNRA). DNRA is an anaerobic respiration process that is known mainly from prokaryotic organisms, and here shown as dissimilatory nitrate reduction pathway used by a eukaryotic phototroph. Similar to large sulfur bacteria and benthic foraminifera, diatoms may respire intracellular NO3− in sediment layers without O2 and NO3−. The rapid depletion of the intracellular NO3− storage, however, implies that diatoms use DNRA to enter a resting stage for long-term survival. Assuming that pelagic diatoms are also capable of DNRA, senescing diatoms that sink through oxygen-deficient water layers may be a significant NH4+ source for anammox, the prevalent nitrogen loss pathway of oceanic oxygen minimum zones.

  • eukaryotic microbiology
  • marine ecology
  • N-cycle
  • nitrate ammonification
  • microalgae

Footnotes

  • 1To whom correspondence should be sent. E-mail: akamp{at}mpi-bremen.de.
  • Author contributions: A.K., D.d.B., G.L., and P.S. designed research; A.K., J.L.N., G.L., and P.S. performed research; A.K., J.L.N., G.L., and P.S. analyzed data; and A.K., D.d.B., G.L., and P.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

Freely available online through the PNAS open access option.

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Diatoms respire nitrate to survive dark and anoxic conditions
Anja Kamp, Dirk de Beer, Jana L. Nitsch, Gaute Lavik, Peter Stief
Proceedings of the National Academy of Sciences Mar 2011, 201015744; DOI: 10.1073/pnas.1015744108

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Diatoms respire nitrate to survive dark and anoxic conditions
Anja Kamp, Dirk de Beer, Jana L. Nitsch, Gaute Lavik, Peter Stief
Proceedings of the National Academy of Sciences Mar 2011, 201015744; DOI: 10.1073/pnas.1015744108
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