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Abstract

Diatoms are one of the most ecologically successful classes of photosynthetic marine eukaryotes in the contemporary oceans. Over the past 30 million years, they have helped to moderate Earth’s climate by absorbing carbon dioxide from the atmosphere, sequestering it via the biological carbon pump and ultimately burying organic carbon in the lithosphere1. The proportion of planetary primary production by diatoms in the modern oceans is roughly equivalent to that of terrestrial rainforests2. In photosynthesis, the efficient conversion of carbon dioxide into organic matter requires a tight control of the ATP/NADPH ratio which, in other photosynthetic organisms, relies principally on a range of plastid-localized ATP generating processes3,4,5,6. Here we show that diatoms regulate ATP/NADPH through extensive energetic exchanges between plastids and mitochondria. This interaction comprises the re-routing of reducing power generated in the plastid towards mitochondria and the import of mitochondrial ATP into the plastid, and is mandatory for optimized carbon fixation and growth. We propose that the process may have contributed to the ecological success of diatoms in the ocean.

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Change history

  • 19 August 2015

    Affiliation number 4 was corrected.

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Acknowledgements

This work was supported by grants from Agence Nationale de la Recherche (ANR-12-BIME-0005, DiaDomOil to C.B., D.P. and G.F.; ANR-8NT09567009, Phytadapt to B.B., G.F. and C.B.; ANR-11-LABX- 0011-01, Dynamo to F.R. and P.J.; ANR-11-IDEX-0001-02, PSL Research University and ANR-10-LABX-54, MEMOLIFE to C.B.), the Région Rhône-Alpes (Cible project) to G.F., the Marie Curie Initial Training Network Accliphot (FP7-PEPOPLE-2012-ITN; 316427) to G.F., D.P., S.F. and V.V., an ERC Advanced Award (Diatomite) and the EU MicroB3 project to C.B., the CNRS Défi (ENRS 2013) to G.F. and L.T., and the CEA Bioénergies program to G.F and D.P. P.C., N.B. and B.B acknowledge financial support from the Belgian Fonds de la Recherche Scientifique F.R.S.-F.N.R.S. (F.R.F.C. 2.4597.11, CDR J.0032.15 and Incentive Grant for Scientific Research F.4520). B.B. also acknowledges a post-doctoral fellowship from Rutgers University and J.P. was funded from the COSI ITN project to C.B. Thanks are due to J.-L. Putaux and C. Lancelon-Pin for help with electron microscopy, to L. Moyet for technical support for the in vivo NMR analysis, to A. E. Allen for the AOX antibody, and to A. Falciatore and F. Barneche for critical reading the manuscript.

Author information

Affiliations

  1. Génétique et Physiologie des Microalgues, Département des Sciences de la vie and PhytoSYSTEMS, Université de Liège, B-4000 Liège, Belgium

    • Benjamin Bailleul
    • , Nicolas Berne
    •  & Pierre Cardol
  2. Environmental Biophysics and Molecular Ecology Program, Departments of Marine and Coastal Sciences and of Earth and Planetary Sciences, Rutgers University, New Brunswick, New Jersey 08901, USA

    • Benjamin Bailleul
    •  & Paul G. Falkowski
  3. Institut de Biologie Physico-Chimique (IBPC), UMR 7141, Centre National de la Recherche Scientifique (CNRS), Université Pierre et Marie Curie, 13 Rue Pierre et Marie Curie, F-75005 Paris, France

    • Benjamin Bailleul
    • , Fabrice Rappaport
    •  & Pierre Joliot
  4. Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), CNRS UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France

    • Benjamin Bailleul
    • , Omer Murik
    • , Judit Prihoda
    • , Atsuko Tanaka
    • , Leila Tirichine
    •  & Chris Bowler
  5. Laboratoire de Physiologie Cellulaire et Végétale, UMR 5168, Centre National de la Recherche Scientifique (CNRS), Commissariat à l’Energie Atomique et aux Energies Alternatives (CEA), Université Grenoble Alpes, Institut National Recherche Agronomique (INRA), Institut de Recherche en Sciences et Technologies pour le Vivant (iRTSV), CEA Grenoble, F-38054 Grenoble cedex 9, France

    • Dimitris Petroutsos
    • , Richard Bligny
    • , Serena Flori
    • , Denis Falconet
    •  & Giovanni Finazzi
  6. Fermentalg SA, F-33500 Libourne, France

    • Valeria Villanova
  7. Institute for Integrative Biology of the Cell (I2BC), Commissariat à l’Energie Atomique et aux Energies Alternatives (CEA), Centre National de la Recherche Scientifique (CNRS), Université Paris-Sud, Institut de Biologie et de Technologie de Saclay, F-91191 Gif-sur-Yvette cedex, France

    • Anja Krieger-Liszkay
  8. Istituto di Biofisica, Consiglio Nazionale delle Ricerche, Via Celoria 26, I-20133 Milan, Italy

    • Stefano Santabarbara

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Contributions

B.B., L.T., C.B. and G.F. designed the study. B.B., N.B., O.M., D.P., J.P., A.T., V.V., R.B., S.F., D.F., A.K-L, F.R., P.J., L.T., P.C. and G.F. performed experiments. B.B., N.B., O.M., D.P., R.B., A.K.-L., S.S., F.R., P.J., L.T., P.F., P.C., C.B. and G.F. analysed the data. B.B., C.B. and G.F. wrote the manuscript, and all authors revised and approved it.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Benjamin Bailleul or Chris Bowler or Giovanni Finazzi.

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DOI

https://doi.org/10.1038/nature14599

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