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.
Subscribe to Journal
Get full journal access for 1 year
only $3.83 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Béjà, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000)
Béjà, O., Spudich, E. N., Spudich, J. L., Leclerc, M. & DeLong, E. F. Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001)
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)
Man-Aharonovich, D. et al. Characterization of RS29, a blue-green proteorhodopsin variant from the Red Sea. Photochem. Photobiol. Sci. 3, 459–462 (2004)
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)
Sabehi, G. et al. Novel Proteorhodopsin variants from the Mediterranean and Red Seas. Environ. Microbiol. 5, 842–849 (2003)
Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004)
Morris, R. M. et al. SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420, 806–810 (2002)
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)
Giovannoni, S. J. et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309, 1242–1245 (2005)
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)
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)
Man, D. et al. Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 22, 1725–1731 (2003)
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)
Ram, R. J. et al. Community proteomics of a natural microbial biofilm. Science 308, 1915–1920 (2005)
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)
Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: The unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998)
Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983)
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)
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)
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)
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.
The HTCC1062 proteorhodopsin gene sequence has been deposited in GenBank under accession number CP000084. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
About this article
Cite this article
Giovannoni, S., Bibbs, L., Cho, J. et al. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85 (2005). https://doi.org/10.1038/nature04032
Biology & Philosophy (2020)
Photochemical characterization of flavobacterial rhodopsin: The importance of the helix E region for heat stability
Biochimica et Biophysica Acta (BBA) - Bioenergetics (2020)
Response of bacterial communities from Kongsfjorden (Svalbard, Arctic Ocean) to macroalgal polysaccharide amendments
Marine Environmental Research (2020)
Dynamic marine viral infections and major contribution to photosynthetic processes shown by spatiotemporal picoplankton metatranscriptomes
Nature Communications (2019)
Microevolution and Adaptive Strategy of Psychrophilic Species Flavobacterium bomense sp. nov. Isolated From Glaciers
Frontiers in Microbiology (2019)