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Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation

  1. Andrew E. Allen * , † ,
  2. Julie LaRoche ‡ , § ,
  3. Uma Maheswari *,
  4. Markus Lommer ‡ ,
  5. Nicolas Schauer ,
  6. Pascal J. Lopez *,
  7. Giovanni Finazzi ‖ ,
  8. Alisdair R. Fernie , and
  9. Chris Bowler * , § , **
  1. *Centre National de la Recherche Scientifique Unite Mixte de Recherche 8186, Dept of Biology, Ecole Normale Supérieure, 46 rue d'Ulm, 75005 Paris, France;
  2. ‡Leibniz-Institut für Meereswissenschaften, 24105 Kiel, Germany;
  3. Max Planck Institute of Molecular Plant Physiology, Am Muhlenberg 1, 14476 Potsdam-Golm, Germany;
  4. ‖Centre National de la Recherche Scientifique Unite Mixte de Recherche 7141, Université Paris 6 Institut de Biologie Physico-Chimique, 13 rue Pierre et Marie Curie, 75005 Paris, France; and
  5. **Stazione Zoologica, Villa Comunale, I 80121 Naples, Italy

  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved May 3, 2008 (received for review December 4, 2007)

Abstract

Marine primary productivity is iron (Fe)-limited in vast regions of the contemporary oceans, most notably the high nutrient low chlorophyll (HNLC) regions. Diatoms often form large blooms upon the relief of Fe limitation in HNLC regions despite their prebloom low cell density. Although Fe plays an important role in controlling diatom distribution, the mechanisms of Fe uptake and adaptation to low iron availability are largely unknown. Through a combination of nontargeted transcriptomic and metabolomic approaches, we have explored the biochemical strategies preferred by Phaeo dactylum tricornutum at growth-limiting levels of dissolved Fe. Processes carried out by components rich in Fe, such as photosynthesis, mitochondrial electron transport, and nitrate assimilation, were down-regulated. Our results show that this retrenchment is compensated by nitrogen (N) and carbon (C) reallocation from protein and carbohydrate degradation, adaptations to chlorophyll biosynthesis and pigment metabolism, removal of excess electrons by mitochondrial alternative oxidase (AOX) and non-photochemical quenching (NPQ), and augmented Fe-independent oxidative stress responses. Iron limitation leads to the elevated expression of at least three gene clusters absent from the Thalassiosira pseudonana genome that encode for components of iron capture and uptake mechanisms.

Footnotes

  • §To whom correspondence may be addressed. E-mail: jlaroche{at}ifm-geomar.de or cbowler{at}biologie.ens.fr

  • Author contributions: A.E.A., J.L., P.J.L., and C.B. designed research; A.E.A., J.L., U.M., M.L., N.S., and G.F. performed research; J.L., P.J.L., G.F., A.R.F., and C.B. contributed new reagents/analytic tools; A.E.A., J.L., U.M., M.L., N.S., G.F., and A.R.F. analyzed data; and A.E.A., J.L., and C.B. wrote the paper.

  • ↵ †Present address: J. Craig Venter Institute, 10355 Science Center Drive, San Diego, CA 92121.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession no. GSE8675).

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0711370105/DCSupplemental.

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