Proteorhodopsin in the ubiquitous marine bacterium SAR11

Abstract

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.

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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.

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Acknowledgements

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.

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Correspondence to Stephen J. Giovannoni.

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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.

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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

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