Abstract
Proteorhodopsins (PR) are light-driven proton pumps widely distributed in bacterioplankton. Although they have been thoroughly studied for more than a decade, it is still unclear how the proton motive force (pmf) generated by PR is used in most organisms. Notably, very few PR-containing bacteria show growth enhancement in the light. It has been suggested that the presence of specific functions within a genome may define the different PR-driven light responses. Thus, comparing closely related organisms that respond differently to light is an ideal setup to identify the mechanisms involved in PR light-enhanced growth. Here, we analyzed the transcriptomes of three PR-harboring Flavobacteria strains of the genus Dokdonia: Dokdonia donghaensis DSW-1T, Dokdonia MED134 and Dokdonia PRO95, grown in identical seawater medium in light and darkness. Although only DSW-1T and MED134 showed light-enhanced growth, all strains expressed their PR genes at least 10 times more in the light compared with dark. According to their genomes, DSW-1T and MED134 are vitamin-B1 auxotrophs, and their vitamin-B1 TonB-dependent transporters (TBDT), accounted for 10–18% of all pmf-dependent transcripts. In contrast, the expression of vitamin-B1 TBDT was 10 times lower in the prototroph PRO95, whereas its vitamin-B1 synthesis genes were among the highest expressed. Our data suggest that light-enhanced growth in DSW-1T and MED134 derives from the use of PR-generated pmf to power the uptake of vitamin-B1, essential for central carbon metabolism, including the TCA cycle. Other pmf-generating mechanisms available in darkness are probably insufficient to power transport of enough vitamin-B1 to support maximum growth of these organisms.
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Acknowledgements
We thank Christopher Suffridge for the vitamin-B1 quantification in the growth medium. The manuscript was improved by the comments of five anonymous reviewers and the editor. This work was supported by the Marie Curie Actions–International Outgoing Fellowships (project 253970). Additional funding was provided by the Spanish Ministry of Science and Innovation (project CTM2013-48292-C3-3-R), the National Science Foundation (grants OCE1136818, OCE1335269 and OCE1435666), the Gordon and Betty Moore Foundation Marine Microbiology Initiative award 3779 and the German Research Organization (DFG), Collaborative Research Grant TRR51 Roseobacter.
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LG-C and IW-D conceived and designed the experiments; LG-C and TR performed the experiments; LG-C and JMG analyzed the data; LG-C, JMG, IW-D, JAF and SJ contributed reagents/materials/analysis tools; LG-C, JMG, TR, SAS-W, IW-D and JAF contributed to the writing the manuscript.
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Gómez-Consarnau, L., González, J., Riedel, T. et al. Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria. ISME J 10, 1102–1112 (2016). https://doi.org/10.1038/ismej.2015.196
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DOI: https://doi.org/10.1038/ismej.2015.196
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