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Proteorhodopsin phototrophy in the ocean

Nature volume 411, pages 786–789 (2001)Cite this article

Abstract

Proteorhodopsin1, a retinal-containing integral membrane protein that functions as a light-driven proton pump, was discovered in the genome of an uncultivated marine bacterium; however, the prevalence, expression and genetic variability of this protein in native marine microbial populations remain unknown. Here we report that photoactive proteorhodopsin is present in oceanic surface waters. We also provide evidence of an extensive family of globally distributed proteorhodopsin variants. The protein pigments comprising this rhodopsin family seem to be spectrally tuned to different habitats—absorbing light at different wavelengths in accordance with light available in the environment. Together, our data suggest that proteorhodopsin-based phototrophy is a globally significant oceanic microbial process.

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Figure 1: Laser flash-induced absorbance changes in suspensions of membranes prepared from the prokaryotic fraction of Monterey Bay surface waters.
Figure 2: Laser flash-induced transients at 500 nm of a Monterey Bay bacterioplankton membrane preparation.
Figure 3: Phylogenetic analysis of the inferred amino-acid sequence of cloned proteorhodopsin genes.
Figure 4: Multiple alignment of proteorhodopsin amino-acid sequences.
Figure 5: Absorption spectra of retinal-reconstituted proteorhodopsins in E. coli membranes.

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Accession codes

Accessions

GenBank/EMBL/DDBJ

Data deposits

The sequences have been deposited with GenBank under accession numbers AF349976–AF350003.

References

  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. Oesterhelt, D. & Stoeckenius, W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature 233, 149– 152 (1971).

    CAS  Google Scholar 

  3. Henderson, R. & Unwin, P. N. Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257, 28– 32 (1975).

    Article  ADS  CAS  Google Scholar 

  4. Danon, A. & Stoeckenius, W. Photophosphorylation in Halobacterium halobium. Proc. Natl Acad. Sci. USA 71, 1234– 1238 (1974).

    Article  ADS  CAS  Google Scholar 

  5. Mullins, T. D., Britcshgi, T. B., Krest, R. L. & Giovannoni, S. J. Genetic comparisons reveal the same unknown bacterial lineages in Atlantic and Pacific bacterioplankton communities. Limnol. Oceanogr. 40, 148– 158 (1995).

    Article  ADS  CAS  Google Scholar 

  6. Sasaki, J. & Spudich, J. L. The transducer protein HtrII modulates the lifetimes of sensory rhodopsin II photointermediates. Biophys. J. 75, 2435– 2440 (1998).

    Article  ADS  CAS  Google Scholar 

  7. Spudich, J. L., Yang, C. S., Jung, K. H. & Spudich, E. N. Retinylidene proteins: Structures and functions from archaea to humans. Annu. Rev. Cell Dev. Biol. 16, 365– 392 (2000).

    Article  CAS  Google Scholar 

  8. Neugebauer, D. C., Zingsheim, H. P. & Oesterhelt, D. Biogenesis of purple membrane in halobacteria. Methods Enzymol. 97, 218– 226 (1983).

    Article  CAS  Google Scholar 

  9. Michel, H. & Oesterhelt, D. Electrochemical proton gradient across the cell membrane of Halobacterium halobium: effect of N,N′-dicyclohexylcarbodiimide, relation to intracellular adenosine triphosphate, adenosine diphosphate, and phosphate concentration, and influence of the potassium gradient. Biochemistry 19, 4607– 4614 (1980).

    Article  CAS  Google Scholar 

  10. 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 

  11. Karl, D. M. & Lukas, R. The Hawaii Ocean Time-series (HOT) program: Background, rationale and field implementation. Deep-Sea Res. 43, 129– 156 (1996).

    ADS  CAS  Google Scholar 

  12. Takahashi, T. et al. Color regulation in the archaebacterial phototaxis receptor phoborhodopsin (sensory rhodopsin II). Biochemistry 29, 8467– 8474 (1990).

    Article  CAS  Google Scholar 

  13. Kirk, J. T. O. in Light and Photosynthesis in Aquatic Ecosystems 104– 134 (Cambridge Univ. Press, Cambridge, 1983).

    Google Scholar 

  14. Bowmaker, J. K. The ecology of visual pigments. Novartis Found. Symp. 224, 21– 31 (1999).

    CAS  PubMed  Google Scholar 

  15. Urbach, E., Scanlan, D. J., Distel, D. L., Waterbury, J. B. & Chisholm, S. W. Rapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J. Mol. Evol. 46, 188– 201 (1998).

    Article  ADS  CAS  Google Scholar 

  16. Moore, L. R., Rocap, G. & Chisholm, S. W. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393, 464– 467 (1998).

    Article  ADS  CAS  Google Scholar 

  17. Palenik, B. Chromatic adaptation in marine Synechococcus strains. Appl. Environ. Microbiol. 67, 991– 994 (2001).

    Article  CAS  Google Scholar 

  18. Ferris, M. J. & Palenik, B. Niche adaptation in ocean cyanobacteria. Nature 396, 226– 228 (1998).

    Article  ADS  CAS  Google Scholar 

  19. Kolber, Z. S., Van Dover, C. L., Niderman, R. A. & Falkowski, P. G. Bacterial photosynthesis in surface waters of the open ocean. Nature 407, 177– 179 (2000).

    Article  ADS  CAS  Google Scholar 

  20. Eilers, H., Pernthaler, J., Glockner, F. O. & Amann, R. Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl. Environ. Microbiol. 66, 3044– 3051 (2000).

    Article  CAS  Google Scholar 

  21. Gonzalez, J. M. et al. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl. Environ. Microbiol. 66, 4237– 4246 (2000).

    Article  CAS  Google Scholar 

  22. Rappé, M. S., Vergin, K. & Giovannoni, S. J. Phylogenetic comparisons of a coastal bacterioplankton community with its counterparts in open ocean and freshwater systems. FEMS Microbiol. Ecol. 33, 219– 232 (2000).

    Article  Google Scholar 

  23. DeLong, E. F. et al. Dibiphytanyl ether lipids in nonthermophilic crenarchaeotes. Appl. Environ. Microbiol. 64, 1133– 1138 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Shimono, K., Iwamoto, M., Sumi, M. & Kamo, N. Functional expression of pharaonis phoborhodopsin in Escherichia coli. FEBS Lett. 420, 54– 56 (1997).

    Article  CAS  Google Scholar 

  25. DeLong, E. F., Taylor, L. T., Marsh, T. L. & Preston, C. M. Visualization and enumeration of marine planktonic archaea and bacteria by using polyribonucleotide probes and fluorescent in situ hybridization. Appl. Environ. Microbiol. 65, 5554– 5563 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank J. Zehr and D. Karl for the HOT samples and the captain and crew of the RV Point Lobos for expert assistance at sea. D. Karl and R. Letellier provided spectral irradiance data. This research was supported by the National Science Foundation (E.F.D.), the NIH (J.L.S.), and the David and Lucile Packard Foundation (E.F.D.).

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Author notes

  1. Oded Béjà, Elena N. Spudich and John L. Spudich: These authors contributed equally to this work

Authors and Affiliations

  1. Monterey Bay Aquarium Research Institute, Moss Landing, 95039, California, USA

    Oded Béjà, Marion Leclerc & Edward F. DeLong

  2. Department of Microbiology and Molecular Genetics, The University of Texas Medical School, Houston, 77030, Texas, USA

    Elena N. Spudich & John L. Spudich

Authors
  1. Oded Béjà
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  2. Elena N. Spudich
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  4. Marion Leclerc
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  5. Edward F. DeLong
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Correspondence to Edward F. DeLong.

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Béjà, O., Spudich, E., Spudich, J. et al. Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001). https://doi.org/10.1038/35081051

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