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Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea

Abstract

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.

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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.

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Acknowledgements

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.

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Correspondence to Edward F. DeLong.

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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 npg.nature.com/reprintsandpermissions. 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)

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Frigaard, NU., Martinez, A., Mincer, T. et al. Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea. Nature 439, 847–850 (2006). https://doi.org/10.1038/nature04435

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