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.

Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea


Planktonic Bacteria, Archaea and Eukarya reside and compete in the ocean's photic zone under the pervasive influence of light. Bacteria in this environment were recently shown to contain photoproteins called proteorhodopsins, thought to contribute to cellular energy metabolism by catalysing light-driven proton translocation across the cell membrane1,2,3,4,5,6,7. So far, proteorhodopsin genes have been well documented only in proteobacteria and a few other bacterial groups. Here we report the presence and distribution of proteorhodopsin genes in Archaea affiliated with the order Thermoplasmatales, in the ocean's upper water column. The genomic context and phylogenetic relationships of the archaeal and proteobacterial proteorhodopsins indicate its probable lateral transfer between planktonic Bacteria and Archaea. About 10% of the euryarchaeotes in the photic zone contained the proteorhodopsin gene adjacent to their small-subunit ribosomal RNA. The archaeal proteorhodopsins were also found in other genomic regions, in the same or in different microbial lineages. Although euryarchaeotes were distributed throughout the water column, their proteorhodopsins were found only in the photic zone. The cosmopolitan phylogenetic distribution of proteorhodopsins reflects their significant light-dependent fitness contributions, which drive the photoprotein's lateral acquisition and retention, but constrain its dispersal to the photic zone.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it


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

Figure 1: Phylogenetic relationships of rhodopsins.
Figure 2: Genetic maps and alignments of fosmid clones from the picoplankton genomic DNA libraries.
Figure 3: Phylogenetic tree of euryarchaeal SSU rRNA sequences from the picoplankton genomic DNA libraries.
Figure 4: Fosmid distribution in the picoplankton genomic DNA libraries.


  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. 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 

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

    Article  ADS  CAS  Google Scholar 

  5. Giovannoni, S. J. et al. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85 (2005)

    Article  ADS  CAS  Google Scholar 

  6. 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 

  7. Sabehi, G. et al. New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol. 3, 1–9 (2005)

    Article  Google Scholar 

  8. Fuhrman, J. A., McCallum, K. & Davis, A. A. Novel major archaebacterial group from marine plankton. Nature 356, 148–149 (1992)

    Article  ADS  CAS  Google Scholar 

  9. DeLong, E. F. Archaea in coastal marine environments. Proc. Natl Acad. Sci. USA 89, 5685–5689 (1992)

    Article  ADS  CAS  Google Scholar 

  10. Massana, R., Murray, A. E., Preston, C. M. & DeLong, E. F. Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl. Environ. Microbiol. 63, 50–56 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Massana, R., DeLong, E. F. & Pedrós-Alió, C. A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl. Environ. Microbiol. 66, 1777–1787 (2000)

    Article  CAS  Google Scholar 

  12. Karner, M. B., DeLong, E. F. & Karl, D. M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507–510 (2001)

    Article  ADS  CAS  Google Scholar 

  13. Pernthaler, A., Preston, C. M., Pernthaler, J., DeLong, E. F. & Amann, R. Comparison of fluorescently labeled oligonucleotide and polynucleotide probes for the detection of pelagic marine Bacteria and Archaea. Appl. Environ. Microbiol. 68, 661–667 (2002)

    Article  CAS  Google Scholar 

  14. DeLong, E. F. Oceans of Archaea. ASM News 69, 503–511 (2003)

    Google Scholar 

  15. Pearson, A., McNichol, A. P., Benitez-Nelson, B. C., Hayes, J. M. & Eglinton, T. I. Origins of lipid biomarkers in Santa Monica Basin surface sediment: A case study using compound-specific Δ14C analysis. Geochim. Cosmochim. Acta 65, 3123–3137 (2001)

    Article  ADS  CAS  Google Scholar 

  16. Wuchter, C., Schouten, S., Boschker, H. T. & Sinninghe Damsté, J. S. Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol. Lett. 219, 203–207 (2003)

    Article  CAS  Google Scholar 

  17. Herndl, G. J. et al. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl. Environ. Microbiol. 71, 2303–2309 (2005)

    Article  CAS  Google Scholar 

  18. Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005)

    Article  ADS  Google Scholar 

  19. Béjà, O. et al. Construction and analysis of bacterial artificial chromosome libraries from a marine microbial assemblage. Environ. Microbiol. 2, 516–529 (2000)

    Article  Google Scholar 

  20. Moreira, D., Rodríguez-Valera, F. & López-García, P. Analysis of a genome fragment of a deep-sea uncultivated Group II euryarchaeote containing 16S rDNA, a spectinomycin-like operon and several energy metabolism genes. Environ. Microbiol. 6, 959–969 (2004)

    Article  CAS  Google Scholar 

  21. Balashov, S. P. et al. Xanthorhodopsin: A proton pump with a light-harvesting carotenoid antenna. Science 309, 2061–2064 (2005)

    Article  ADS  CAS  Google Scholar 

  22. Baliga, N. S. et al. Genome sequence of Haloarcula marismortui: A halophilic archaeon from the Dead Sea. Genome Res. 14, 2221–2234 (2004)

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  24. DeLong, E. F. et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science (in the press)

  25. Giuliano, G., Al-Babili, S. & von Lintig, J. Carotenoid oxygenases: Cleave it or leave it. Trends Plant Sci. 8, 145–149 (2003)

    Article  CAS  Google Scholar 

  26. Ruch, S., Beyer, P., Ernst, H. & Al-Babili, S. Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Mol. Microbiol. 55, 1015–1024 (2005)

    Article  CAS  Google Scholar 

  27. Woese, C. R. A new biology for a new century. Microbiol. Mol. Biol. Rev. 68, 173–186 (2004)

    Article  CAS  Google Scholar 

  28. Ochman, H., Lerat, E. & Daubin, V. Examining bacterial species under the specter of gene transfer and exchange. Proc. Natl Acad. Sci. USA 102 (Suppl. 1), 6595–6599 (2005)

    Article  ADS  CAS  Google Scholar 

  29. Ochman, H., Lerat, E., Daubin, V. & Moran, N. A. Evolutionary origins of genomic repertoires in bacteria. PLoS Biol. 3, e130 (2005)

    Article  Google Scholar 

  30. Suzuki, M. T. et al. Phylogenetic screening of ribosomal RNA gene-containing clones in bacterial artificial chromosome (BAC) libraries from different depths in Monterey Bay. Microb. Ecol. 48, 473–488 (2004)

    Article  CAS  Google Scholar 

Download references


We thank C. Preston and L. Christianson for assistance in the initial sample collection and fosmid library construction; P. Richardson, K. Barry, S. Pitluck and the Joint Genome Institute production team for their help in sequencing; and D. Karl at the University of Hawaii, and the Hawaii Ocean Time Series team, who made sample collection possible. This research was supported by a grant to E.F.D. from The Gordon and Betty Moore Foundation under the Marine Microbiology Initiative program, and a National Science Foundation Microbial Observatory grant to E.F.D. Terminus sequencing of large-insert clones was performed by the Joint Genome Institute (Walnut Creek, California) under the auspices of the US Department of Energy's Office of Science, Biological, and Environmental Research Microbial Genomes Program. Author Contributions E.F.D. made the initial bioinformatic observation of linkage between proteorhodopsin and archaeal genes. N.-U.F. and E.F.D. developed the concepts of the paper together. N.-U.F. performed the experiments, except the proteorhodopsin expression experiments, which were performed by A.M. T.J.M. participated in obtaining and analysing the SSU rRNA sequences. N.-U.F. wrote the first draft of the paper, which was completed by N.-U.F. and E.F.D. together.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Edward F. DeLong.

Ethics declarations

Competing interests

The sequences reported here have been deposited in GenBank under accession numbers DQ257435, DQ257434, DQ156349, DQ156348 (fosmids HF10_3D09, HF70_19B12, HF70_39H11 and HF70_59C08), DQ156379–DQ156483 (SSU rRNA), DQ156350–DQ156363, DU708536–DU708556 (fosmid termini) and DQ156364–DQ156378 (proteorhodopsin sequences). Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Tables 1–4 and Supplementary Figures 1–4 (DOC 1513 kb)

Supplementary Notes 2

Genes and proteins discussed in the main text. (DOC 27 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Frigaard, NU., Martinez, A., Mincer, T. et al. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439, 847–850 (2006).

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