Letter | Published:

Bacterial photosynthesis in surface waters of the open ocean

Nature volume 407, pages 177179 (14 September 2000) | Download Citation

Subjects

Abstract

The oxidation of the global ocean by cyanobacterial oxygenic photosynthesis, about 2,100 Myr ago1, is presumed to have limited anoxygenic bacterial photosynthesis to oceanic regions that are both anoxic and illuminated2,3. The discovery of oxygen-requiring photosynthetic bacteria about 20 years ago4 changed this notion, indicating that anoxygenic bacterial photosynthesis could persist under oxidizing conditions. However, the distribution of aerobic photosynthetic bacteria in the world oceans, their photosynthetic competence and their relationship to oxygenic photoautotrophs on global scales are unknown. Here we report the first biophysical evidence demonstrating that aerobic bacterial photosynthesis is widespread in tropical surface waters of the eastern Pacific Ocean and in temperate coastal waters of the northwestern Atlantic. Our results indicate that these organisms account for 2–5% of the photosynthetic electron transport in the upper ocean.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    & Paleosols and the evolution of atmospheric oxygen: a critical review. Am. J. Sci. 298, 621–672 (1998).

  2. 2.

    & Aquatic Photosynthesis (Blackwell, Oxford, 1997).

  3. 3.

    , & (eds). Anoxygenic Photosynthetic Bacteria (Kluwer, Dordrecht, 1995).

  4. 4.

    , & Distribution of aeorobic bacteria which contain bacteriochlorophyll a. Appl. Environ. Microbiol. 38, 43– 48 (1979).

  5. 5.

    , , , & Occurrence of bacteriochlorophyll a in a strain of aerobic heterotrophic bacterium. Agric. Biol. Chem. 42, 1627–1628 (1987).

  6. 6.

    , & Aerobic Photosynthetic Bacteria. (Springer, Berlin, 1989).

  7. 7.

    in Anoxygenic Photosynthetic Bacteria (eds. Blankenship, R. E., Madigan, M. T. & Bauer, C. E.) 105–122 (Kluwer, Dordrecht, 1995).

  8. 8.

    et al. The phylogeny of purple bacteria; The alpha subdivision. Syst. Appl. Microbiol. 5, 315–326 (1984).

  9. 9.

    et al. Phylogenetic positions of novel areobic, bacteriochlorophyll a containing bacteria and description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. Int. J.Syst. Bacteriol 44, 427–434 ( 1994).

  10. 10.

    et al. DNA relatedness and chemotaxonomic feature of aerobic bacteriochlorophyll-containing bacteria isolated from coast of Australia. J. Gen. Appl. Microbiol. 40, 287–296 ( 1994).

  11. 11.

    & Aeorobic anoxygenic phototrophic bacteria. Microbiol. Mol. Biol. Rev. 62, 695–724 (1998).

  12. 12.

    , , , & In vivo states and function of carotenoids in an aerobic photosynthetic bacterium, Erythrobacter longus. Photosynth. Res. 31, 21–30 (1992).

  13. 13.

    , & Kinetics of electron transfer between the tetrahemic cytochrome and special pair in isolated reaction centers of Roseobacter denitrificans. Photosynth. Res. 55, 331–335 (1998).

  14. 14.

    , , & Photo-induced cyclic electron transfer involving cytochrome bc1 complex and reaction center in the obligate aerobic phototroph Roseobacter denitrificans . Eur. J. Biochem. 267, 422– 433 (2000).

  15. 15.

    Utilization of the light energy by the strictly aerobic bacterium Erythrobacter sp. OCh114. J. Gen. Appl. Microbiol. 30, 1313–1320 (1984).

  16. 16.

    , , & Citromicrobium bathymonarium, a novel aeorobic bacterium isolated from deep sea hydrothermal vent plume waters that contains photosynthetic pigment-protein complexes. J. Bacteriol. 181, 4517– 4525 (1999).

  17. 17.

    , & Origins of photosynthesis. Nature 373, 479–480 (1995).

  18. 18.

    , , & Light at deep sea hydrothermal vents. Geophys. Res. Lett. 23, 2049–2052 (1996).

  19. 19.

    , & Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim. Biophys. Acta 1367, 88–106 (1998).

  20. 20.

    , & in The photosystems: Stucture, Function and Molecular Biology (ed. Barber, J. R.) 295–348 (Elsevier, New York, 1992).

  21. 21.

    Cell cycle regulation and the timing of chromosome replication in marine Synechococcus (cyanobacteria) during light- and nitrogen-limited growth. J. Phycol. 36, 120–126 (2000).

  22. 22.

    & Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283, 840–843 ( 1999).

  23. 23.

    & Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol. Oceanogr. 38, 1646–1665 (1993).

  24. 24.

    & Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynt. Res. 53, 229–241 (1997).

  25. 25.

    , , , & Distribution and physiology of aerobic bacteria containing bacteriochlorophyll a on the east and west coast of Australia. Appl. Environ. Microbiol. 57, 295– 300 (1991).

  26. 26.

    & Isolation of aerobic anoxygenic photosynthetic bacteria from black smoker plume waters of the Juan de Fuca Ridge in the Pacific Ocean. Appl. Environ. Microbiol. 64, 337 –341 (1998).

  27. 27.

    in Photobiology of Microorganisms (ed. Halldall, P.) 95– 133 (Wiley-Interscience, London, 1970).

  28. 28.

    in Algal Physiology and Biochemistry (ed. Stewart, W. D. P.) 531– 599 (Blackwell Scientific, Berkeley, 1974).

Download references

Acknowledgements

This research was support by the National Science Foundation and the Office of Naval Research. We thank C. Vetriani, R. Lutz, J. Henderson, G. Ananyev and D. Klimov for technical assistance and the crew of the Alvin for their cooperation. We thank P. Minnett for the SST data.

Author information

Affiliations

  1. *Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences, Rutgers University , New Brunswick, New Jersey 08901-8521, USA

    • Z. S. Kolber
    •  & P. G. Falkowski
  2. †Biology Department, College of William & Mary, Williamsburg, Virginia 23187, USA

    • C. L. Van Dover
  3. ‡Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, New Jersey 08854-8082, USA

    • R. A. Niederman

Authors

  1. Search for Z. S. Kolber in:

  2. Search for C. L. Van Dover in:

  3. Search for R. A. Niederman in:

  4. Search for P. G. Falkowski in:

Corresponding author

Correspondence to P. G. Falkowski.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/35025044

Further reading

Comments

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.