Abstract
Metagenomic analyses have revealed widespread and diverse retinal-binding rhodopsin proteins (named proteorhodopsins) among numerous marine bacteria and archaea, which has challenged the notion that solar energy can only enter marine ecosystems by chlorophyll-based photosynthesis. Most marine proteorhodopsins share structural and functional similarities with archaeal bacteriorhodopsins, which generate proton motive force via light-activated proton pumping, thereby ultimately powering ATP production. This suggests an energetic role for proteorhodopsins. However, results from a growing number of investigations do not readily fit this model, which indicates that proteorhodopsins could have a range of physiological functions.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Azam, F. et al. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).
Fuhrman, J. A. & Azam, F. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters — evaluation and field results. Mar. Biol. 66, 109–120 (1982).
Beja, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000).
Karl, D. M. Microbiological oceanography: hidden in a sea of microbes. Nature 415, 590–591 (2002).
Kolber, Z. S., Van Dover, C. L., Niederman, R. A. & Falkowski, P. G. Bacterial photosynthesis in surface waters of the open ocean. Nature 407, 177–179 (2000).
Moran, M. A. & Miller, W. L. Resourceful heterotrophs make the most of light in the coastal ocean. Nature Rev. Microbiol. 5, 792–800 (2007).
Giovannoni, S. J. & Rappe, M. Evolution, Diversity, and Molecular Ecology of Marine Prokaryotes (ed. Kirchman, D. L.) 47–84 (Wiley–Liss, New York, 2000).
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).
Martinez, A., Bradley, A. S., Waldbauer, J. R., Summons, R. E. & DeLong, E. F. Proteorhodopsin photosystem gene expression enables photophosphorylation in a heterologous host. Proc. Natl Acad. Sci. USA 104, 5590–5595 (2007).
Giovannoni, S. J. et al. Proteorhodopsin in the ubiquitous marine bacterium SAR11. Nature 438, 82–85 (2005).
Frigaard, N.-U., Martinez, A., Mincer, T. J. & DeLong, E. F. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439, 847–850 (2006).
McCarren, J. & DeLong, E. F. Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environ. Microbiol. 9, 846–858 (2007).
Stingl, U., Desiderio, R. A., Cho, J.-C., Vergin, K. L. & Giovannoni, S. J. The SAR92 clade: an abundant coastal clade of culturable marine bacteria possessing proteorhodopsin. Appl. Environ. Microbiol. 73, 2290–2296 (2007).
Moran, M. A. et al. Ecological genomics of marine roseobacters. Appl. Environ. Microbiol. 73, 4559–4569 (2007).
Gomez-Consarnau, L. et al. Light stimulates growth of proteorhodopsin-containing marine Flavobacteria. Nature 445, 210–213 (2007).
Balashov, S. P. et al. Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309, 2061–2064 (2005).
Mongodin, E. F. et al. The genome of Salinibacter ruber: convergence and gene exchange among hyperhalophilic bacteria and archaea. Proc. Natl Acad. Sci. USA 102, 18147–18152 (2005).
Sharma, A. K., Zhaxybayeva, O., Papke, R. T. & Doolittle, W. F. Actinorhodopsins: proteorhodopsin-like gene sequences found predominantly in non-marine environments. Environ. Microbiol. 10, 1039–1056 (2008).
Brown, L. S. & Jung, K. H. Bacteriorhodopsin-like proteins of eubacteria and fungi: the extent of conservation of the haloarchaeal proton-pumping mechanism. Photochem. Photobiol. Sci. 5, 538–546 (2006).
Giovannoni, S. J. et al. The small genome of an abundant coastal ocean methylotroph. Environ. Microbiol. 3 Apr 2008 (doi:10.1111/j.1462-2920.2008.01598.x).
Sharma, A. K., Spudich, J. L. & Doolittle, W. F. Microbial rhodopsins: functional versatility and genetic mobility. Trends Microbiol. 14, 463–469 (2006).
Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through Eastern Tropical Pacific. PloS Biol. 5, 398–431 (2007).
Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).
Campbell, B. J., Waidner, L. A., Cottrell, M. T. & Kirchman, D. L. Abundant proteorhodopsin genes in the North Atlantic ocean. Environ. Microbiol. 10, 99–109 (2008).
Sabehi, G. et al. New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol. 3, 1409–1417 (2005).
Cottrell, M. T., Mannino, A. & Kirchman, D. L. Aerobic anoxygenic phototrophic bacteria in the Mid-Atlantic Bight and the North Pacific Gyre. Appl. Environ. Microbiol. 72, 557–564 (2006).
Sabehi, G. et al. Adaptation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Seas. ISME J. 1, 48–55 (2007).
Schwalbach, M. S. & Fuhrman, J. A. Wide-ranging abundances of aerobic anoxygenic phototrophic bacteria in the world ocean revealed by epifluorescence microscopy and quantitative PCR. Limnol. Oceanogr. 50, 620–628 (2005).
Spudich, J. L. Protein–protein interaction converts a proton pump into a sensory receptor. Cell 79, 747–750 (1994).
Man, D. et al. Diversification and spectral tuning in marine proteorhodopsins. EMBO J. 22, 1725–1731 (2003).
Stingl, U., Tripp, H. J. & Giovannoni, S. J. Improvements of high-throughput culturing yielded novel SAR11 strains and other abundant marine bacteria from the Oregon coast and the Bermuda Atlantic Time Series study site. ISME J. 1, 361–371 (2007).
Man-Aharonovich, D. et al. Characterization of RS29, a blue–green proteorhodopsin variant from the Red Sea. Photochem. Photobiol. Sci. 3, 459–462 (2004).
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).
Spudich, J. L. The multitalented microbial sensory rhodopsins. Trends Microbiol. 14, 480–487 (2006).
Beja, O., Spudich, E. N., Spudich, J. L., Leclerc, M. & De Long, E. F. Proteorhodopsin phototrophy in the ocean. Nature 411, 786–789 (2001).
Spudich, J. L. & Jung, K. H. in Handbook of Photosensory Receptors (eds Briggs, W. & Spudich, J. L.) 1–24 (Wiley-VCH, Weinheim, 2005).
Anton, J. et al. Salinibacter ruber gen. nov., sp nov., a novel, extremely halophilic member of the Bacteria from saltern crystallizer ponds. Int. J. Syst. Evol. Microbiol. 52, 485–491 (2002).
Giovannoni, S. J. et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309, 1242–1245 (2005).
Schwalbach, M. S., Brown, M. & Fuhrman, J. A. Impact of light on marine bacterioplankton community structure. Aquat. Microb. Ecol. 39, 235–245 (2005).
Church, M. J., Ducklow, H. W. & Karl, D. M. Light dependence of [3H]leucine incorporation in the oligotrophic North Pacific ocean. Appl. Environ. Microbiol. 70, 4079–4087 (2004).
Michelou, V. K., Cottrell, M. T. & Kirchman, D. L. Light-stimulated bacterial production and amino acid assimilation by cyanobacteria and other microbes in the North Atlantic ocean. Appl. Environ. Microbiol. 73, 5539–5546 (2007).
Zubkov, M., Tarran, G. A. & Fuchs, B. M. Depth related amino acid uptake by Prochlorococcus cyanobacteria in the Southern Atlantic tropical gyre. FEMS Microbiol. Ecol. 50, 153–161 (2004).
Lami, R. et al. High abundances of aerobic anoxygenic photosynthetic bacteria in the South Pacific ocean. Appl. Environ. Microbiol. 73, 4198–4205 (2007).
De Long, E. F. & Karl, D. M. Genomic perspectives in microbial oceanography. Nature 437, 336–342 (2005).
Sabehi, G., Beja, O., Suzuki, M. T., Preston, C. M. & DeLong, E. F. Different SAR86 subgroups harbour divergent proteorhodopsins. Environ. Microbiol. 6, 903–910 (2004).
Sabehi, G. et al. Novel proteorhodopsin variants from the Mediterranean and Red Seas. Environ. Microbiol. 5, 842–849 (2003).
Kirchman, D. L. Limitation of bacterial growth by dissolved organic matter in the subarctic Pacific. Mar. Ecol. Prog. Ser. 62, 47–54 (1990).
Church, M. J., Hutchins, D. A. & Ducklow, H. W. Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl. Environ. Microbiol. 66, 455–466 (2000).
Kirchman, D. L. et al. Carbon versus iron limitation of bacterial growth in the California upwelling regime. Limnol. Oceanogr. 45, 1681–1688 (2000).
Van Wambeke, F. et al. Factors limiting heterotrophic bacterial production in the southern Pacific Ocean. Biogeosci. Discuss. 4, 3799–3828 (2007).
Pomeroy, L. R., Sheldon, J. E., Sheldon, W. M. J. & Peters, F. Limits to growth and respiration of bacterioplankton in the Gulf of Mexico. Mar. Ecol. Prog. Ser. 117, 259–268 (1995).
Zohary, T. & Robarts, R. D. Experimental study of microbial P-limitation in the eastern Mediterranean. Limnol. Oceanogr. 43, 387–395 (1998).
Thingstad, T. F. et al. Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309, 1068–1071 (2005).
Cotner, J. B., Ammerman, J. W., Peele, E. R. & Bentzen, E. Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquat. Microb. Ecol. 13, 141–149 (1997).
Pakulski, J. D. et al. Iron stimulation of Antarctic bacteria. Nature 383, 133–134 (1996).
Cochlan, W. P. The heterotrophic bacterial response during a mesoscale iron enrichment experiment (IronEx II) in the eastern equatorial Pacific Ocean. Limnol. Oceanogr. 46, 428–435 (2001).
Oesterhelt, D. & Krippahl, G. Phototrophic growth of halobacteria and its use for isolation of photosynthetically-deficient mutants. Ann. Microbiol. (Paris) 134B, 137–150 (1983).
Jochem, F. J. Dark survival strategies in marine phytoplankton assessed by cytometric measurement of metabolic activity with fluorescein diacetate. Mar. Biol. 135, 721–728 (1999).
Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).
Lakatos, M., Lanyi, J. K., Szakacs, J. & Varo, G. The photochemical reaction cycle of proteorhodopsin at low pH. Biophys. J. 84, 3252–3256 (2003).
Acknowledgements
The authors thank J. Spudich and the anonymous reviewers for their helpful comments, especially on photoregulation and sensory rhodopsins, and D. Rusch for assistance with the GOS data and recalculating the percentage of PR versus recA. This work was supported by NSF Biological Oceanography and Microbial Observatory grants 0527034, 0648581 and 0703159.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Related links
Related links
DATABASES
Entrez Genome Project
FURTHER INFORMATION
Rights and permissions
About this article
Cite this article
Fuhrman, J., Schwalbach, M. & Stingl, U. Proteorhodopsins: an array of physiological roles?. Nat Rev Microbiol 6, 488–494 (2008). https://doi.org/10.1038/nrmicro1893
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrmicro1893
This article is cited by
-
High-resolution metagenomic reconstruction of the freshwater spring bloom
Microbiome (2023)
-
A comparative study reveals the relative importance of prokaryotic and eukaryotic proton pump rhodopsins in a subtropical marginal sea
ISME Communications (2023)
-
High diversity of benthic cyanobacterial mats on coral reefs of Koh Tao, Gulf of Thailand
Coral Reefs (2023)
-
Decoupling of respiration rates and abundance in marine prokaryoplankton
Nature (2022)
-
Light stimulates anoxic and oligotrophic growth of glacial Flavobacterium strains that produce zeaxanthin
The ISME Journal (2021)