This article has been updated


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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Change history

  • 19 August 2015

    Affiliation number 4 was corrected.


  1. 1.

    The evolution of modern eukaryotic phytoplankton. Science 305, 354–360 (2004)

  2. 2.

    , , & Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998)

  3. 3.

    Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant Biol. 58, 199–217 (2007)

  4. 4.

    The water–water cycle as alternative photon and electron sinks. Phil. Trans. R. Soc. Lond. B 355, 1419–1431 (2000)

  5. 5.

    et al. An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc. Natl Acad. Sci. USA 105, 7881–7886 (2008)

  6. 6.

    & A photoprotective role of O2 as an alternative electron sink in photosynthesis? Curr. Opin. Plant Biol. 5, 193–198 (2002)

  7. 7.

    , , & Comparison of the H+/ATP ratios of the H+-ATP synthases from yeast and from chloroplast. Proc. Natl Acad. Sci. USA 109, 11150–11155 (2012)

  8. 8.

    Photosynthesis of ATP-electrons, proton pumps, rotors, and poise. Cell 110, 273–276 (2002)

  9. 9.

    & Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability. Photosynth. Res. 117, 449–459 (2013)

  10. 10.

    Oxygen reduction and optimum production of ATP in photosynthesis. Nature 256, 599–600 (1975)

  11. 11.

    & Photoreduction of O2 primes and replaces CO2 assimilation. Plant Physiol. 58, 336–340 (1976)

  12. 12.

    Photosynthetic oxygen exchange. Annu. Rev. Plant Physiol. 36, 27–53 (1985)

  13. 13.

    et al. Chloroplast-mitochondria cross-talk in diatoms. J. Exp. Bot. 63, 1543–1557 (2012)

  14. 14.

    et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239–244 (2008)

  15. 15.

    , & The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J. Proteome Res. 10, 5338–5353 (2011)

  16. 16.

    Energy conversion in the functional membrane of photosynthesis. Analysis by light pulse and electric pulse methods. The central role of the electric field. Biochim. Biophys. Acta 505, 355–427 (1979)

  17. 17.

    & Characterization of linear and quadratic electrochromic probes in Chlorella sorokiniana and Chlamydomonas reinhardtii. Biochim. Biophys. Acta 975, 355–360 (1989)

  18. 18.

    & Effect of the transmembrane electric field on the photochemical and quenching properties of photosystem II in vivo. Biochim. Biophys. Acta 423, 479–498 (1976)

  19. 19.

    & In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetics effects on cytochrome b6f turnover. Biochemistry 37, 9999–10005 (1998)

  20. 20.

    , , , & Light-induced responses of oxygen photo-reduction, reactive oxygen species production and scavenging in two diatom species. J. Phycol. 46, 1206–1217 (2010)

  21. 21.

    et al. The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism. Plant J. 65, 15–26 (2011)

  22. 22.

    , & Restoration of phototrophic growth in a mutant of Chlamydomonas reinhardtii in which the chloroplast atpB gene of the ATP synthase has a deletion: an example of mitochondria-dependent photosynthesis. Proc. Natl Acad. Sci. USA 85, 1344–1348 (1988)

  23. 23.

    et al. Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc. Natl Acad. Sci. USA 106, 15979–15984 (2009)

  24. 24.

    et al. Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 26, 3036–3050 (2014)

  25. 25.

    , , , & Plasticity and robustness of pattern formation in the model diatom Phaeodactylum tricornutum. New Phytol. 182, 429–442 (2009)

  26. 26.

    in Culture of Marine Invertebrate Animals (eds & ) 26–60 (Plenum, 1975)

  27. 27.

    , , , & Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol. 125, 1919–1929 (2001)

  28. 28.

    & Inhibition of ribulose diphosphate carboxylase by cyanide. Inactive ternary complex of enzyme, ribulose diphosphate, and cyanide. J. Biol. Chem. 244, 55–59 (1969)

  29. 29.

    & Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol. 28, 131–140 (1987)

  30. 30.

    , & Assay and inhibitors of spinach superoxide dismutase. Agric. Biol. Chem. 38, 471–473 (1974)

  31. 31.

    & Flash induced 529 nm absorption change in green algae. Biochim. Biophys. Acta 357, 267–284 (1974)

  32. 32.

    , & Temperature dependence of the reduction of p-700+ by tightly bound plastocyanin in vivo. Biochemistry 48, 10457–10466 (2009)

  33. 33.

    Kinetic analysis of P-700 photoconversion: effect of secondary electron donation and plastocyanin inhibition. Arch. Biochem. Biophys. 217, 536–545 (1982)

  34. 34.

    , , & Electrochromism: a useful probe to study algal photosynthesis. Photosynth. Res. 106, 179–189 (2010)

  35. 35.

    et al. A new setup for in vivo fluorescence imaging of photosynthetic activity. Photosynth. Res. 102, 85–93 (2009)

  36. 36.

    , & The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87–92 (1989)

  37. 37.

    & Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth. Res. 25, 173–186 (1990)

  38. 38.

    & O2 uptake in the light in Chlamydomonas. Plant Physiol. 79, 225–230 (1985)

  39. 39.

    et al. A membrane inlet mass spectrometer for rapid and high-precision determination of N2, O2, and Ar in environmental water samples. Anal. Chem. 66, 4166–4170 (1994)

  40. 40.

    et al. Accumulation of 2-C-methyl-d-erythritol 2,4-cyclodiphosphate in illuminated plant leaves at supraoptimal temperatures reveals a bottleneck of the prokaryotic methylerythritol 4-phosphate pathway of isoprenoid biosynthesis. Plant Cell Environ. 32, 82–92 (2009)

  41. 41.

    & NMR and plant metabolism. Curr. Opin. Plant Biol. 4, 191–196 (2001)

  42. 42.

    & Valve morphogenesis in the centric diatom Rhizosolenia setigera (Bacillariophyceae, Centrales) and its taxonomic implications. Eur. J. Phycol. 39, 93–104 (2004)

  43. 43.

    et al. Gene silencing in the marine diatom Phaeodactylum tricornutum. Nucleic Acids Res. 37, e96 (2009)

  44. 44.

    , , , & Transformation of nonselectable reporter genes in marine diatoms. Mar. Biotechnol. (NY) 1, 239–251 (1999)

Download references


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


  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


  1. Search for Benjamin Bailleul in:

  2. Search for Nicolas Berne in:

  3. Search for Omer Murik in:

  4. Search for Dimitris Petroutsos in:

  5. Search for Judit Prihoda in:

  6. Search for Atsuko Tanaka in:

  7. Search for Valeria Villanova in:

  8. Search for Richard Bligny in:

  9. Search for Serena Flori in:

  10. Search for Denis Falconet in:

  11. Search for Anja Krieger-Liszkay in:

  12. Search for Stefano Santabarbara in:

  13. Search for Fabrice Rappaport in:

  14. Search for Pierre Joliot in:

  15. Search for Leila Tirichine in:

  16. Search for Paul G. Falkowski in:

  17. Search for Pierre Cardol in:

  18. Search for Chris Bowler in:

  19. Search for Giovanni Finazzi in:


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.

Extended data

About this article

Publication history





Further reading


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Newsletter Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing