Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Proteorhodopsin in the ubiquitous marine bacterium SAR11


Proteorhodopsins are light-dependent proton pumps that are predicted to have an important role in the ecology of the oceans by supplying energy for microbial metabolism1,2. Proteorhodopsin genes were first discovered through the cloning and sequencing of large genomic DNA fragments from seawater1. They were later shown to be widely distributed, phylogenetically diverse, and active in the oceans3,4,5,6,7. Proteorhodopsin genes have not been found in cultured bacteria, and on the basis of environmental sequence data, it has not yet been possible to reconstruct the genomes of uncultured bacterial strains that have proteorhodopsin genes. Although the metabolic effect of proteorhodopsins is uncertain, they are thought to function in cells for which the primary mode of metabolism is the heterotrophic assimilation of dissolved organic carbon. Here we report that SAR11 strain HTCC1062 (‘Pelagibacter ubique’)8, the first cultivated member of the extraordinarily abundant SAR11 clade, expresses a proteorhodopsin gene when cultured in autoclaved seawater and in its natural environment, the ocean. The Pelagibacter proteorhodopsin functions as a light-dependent proton pump. The gene is expressed by cells grown in either diurnal light or in darkness, and there is no difference between the growth rates or cell yields of cultures grown in light or darkness.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Phylogenetic relationships between proteorhodopsin amino acid sequences.
Figure 2: Pelagibacter proteorhodopsin peptide (PR3), detected by tandem MALDI mass spectrometry.
Figure 3: Spectroscopy.
Figure 4: Growth characteristics of HTCC1062.

Similar content being viewed by others


  1. Béjà, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000)

    Article  ADS  Google Scholar 

  2. Béjà, O., Spudich, E. N., Spudich, J. L., Leclerc, M. & DeLong, E. F. Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001)

    Article  ADS  Google Scholar 

  3. Sabehi, G., Béjà, O., Suzuki, M. T., Preston, C. M. & DeLong, E. F. Different SAR86 subgroups harbour divergent proteorhodopsins. Environ. Microbiol. 6, 903–910 (2004)

    Article  Google Scholar 

  4. Man-Aharonovich, D. et al. Characterization of RS29, a blue-green proteorhodopsin variant from the Red Sea. Photochem. Photobiol. Sci. 3, 459–462 (2004)

    Article  CAS  Google Scholar 

  5. de la Torre, J. R. et al. Proteorhodopsin genes are distributed among divergent marine bacterial taxa. Proc. Natl Acad. Sci. USA 100, 12830–12835 (2003)

    Article  ADS  CAS  Google Scholar 

  6. Sabehi, G. et al. Novel Proteorhodopsin variants from the Mediterranean and Red Seas. Environ. Microbiol. 5, 842–849 (2003)

    Article  CAS  Google Scholar 

  7. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004)

    Article  ADS  CAS  Google Scholar 

  8. Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002)

    Article  ADS  CAS  Google Scholar 

  9. Rappé, M. S., Connon, S. A., Vergin, K. L. & Giovannoni, S. J. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002)

    Article  ADS  Google Scholar 

  10. Giovannoni, S. J. et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309, 1242–1245 (2005)

    Article  ADS  CAS  Google Scholar 

  11. Field, K. G. et al. Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria. Appl. Environ. Microbiol. 61, 63–70 (1997)

    Google Scholar 

  12. Wang, W. W., Sineshchekov, O. A., Spudich, E. N. & Spudich, J. L. Spectroscopic and photochemical characterization of a deep ocean proteorhodopsin. J. Biol. Chem. 278, 33985–33991 (2003)

    Article  CAS  Google Scholar 

  13. Man, D. et al. Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 22, 1725–1731 (2003)

    Article  CAS  Google Scholar 

  14. Stapels, M. D. & Barofsky, D. F. Complementary use of MALDI and ESI for the HPLC-MS/MS analysis of DNA-binding proteins. Anal. Chem. 76, 5423–5430 (2004)

    Article  CAS  Google Scholar 

  15. Ram, R. J. et al. Community proteomics of a natural microbial biofilm. Science 308, 1915–1920 (2005)

    Article  ADS  CAS  Google Scholar 

  16. Peck, R. F., Johnson, E. A. & Krebs, M. P. Identification of a lycopene β-cyclase required for bacteriorhodopsin biogenesis in the archaeon Halobacterium salinarum. J. Bacteriol. 184, 2889–2897 (2002)

    Article  CAS  Google Scholar 

  17. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: The unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998)

    Article  ADS  CAS  Google Scholar 

  18. Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983)

    Book  Google Scholar 

  19. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    Article  CAS  Google Scholar 

  20. Stapels, M. D., Cho, J. C., Giovannoni, S. J. & Barofsky, D. F. Proteomic analysis of novel marine bacteria using MALDI and ESI mass spectrometry. J. Biomol. Tech. 15, 191–198 (2004)

    PubMed  PubMed Central  Google Scholar 

  21. Perkins, D. N., Pappin, D. J., Creasy, D. M. & Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551–3567 (1999)

    Article  CAS  Google Scholar 

Download references


We thank J. Nibler and the chemistry department at Oregon State University for the use of the Nd:YAG laser and student laser laboratory facilities; W. Hetherington, R. Letelier, B. Geller and O. Béjà for helpful discussions; and E. L. Barofsky for her assistance with MALDI mass spectrometry. This research was supported by the National Science Foundation, Diversa Corporation and the National Institute of Environmental Health Sciences. Author Contributions S.J.G. led the genome sequencing project, provided the bioinformatics analyses and was the primary writer. L.B. and E.J.M. led the DNA sequencing team at Diversa Corporation. J.-C.C., L.J.W. and H.J.T. provided the growth data. M.D.S. and D.F.B. provided the mass spectrometry analysis. R.D. and S.L. performed the light spectroscopy experiments. K.L.V. cloned the proteorhodopsin gene and showed that it was a light-dependent proton pump, with the assistance of R.D. M.S.R. isolated the Pelagibacter.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Stephen J. Giovannoni.

Ethics declarations

Competing interests

The HTCC1062 proteorhodopsin gene sequence has been deposited in GenBank under accession number CP000084. Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Methods, Supplementary Figures 1 and 2 and the Supplementary Tables. (DOC 213 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Giovannoni, S., Bibbs, L., Cho, JC. et al. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85 (2005).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


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.


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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