Abstract
Proteorhodopsin (PR) is a photoprotein that functions as a light-driven proton pump in diverse marine Bacteria and Archaea. Recent studies have suggested that PR may enhance both growth rate and yield in some flavobacteria when grown under nutrient-limiting conditions in the light. The direct involvement of PR, and the metabolic details enabling light-stimulated growth, however, remain uncertain. Here, we surveyed transcriptional and growth responses of a PR-containing marine flavobacterium during carbon-limited growth in the light and the dark. As previously reported (Gómez-Consarnau et al., 2007), Dokdonia strain MED134 exhibited light-enhanced growth rates and cell yields under low carbon growth conditions. Inhibition of retinal biosynthesis abolished the light-stimulated growth response, supporting a direct role for retinal-bound PR in light-enhanced growth. Among protein-coding transcripts, both PR and retinal biosynthetic enzymes showed significant upregulation in the light. Other light-associated proteins, including bacterial cryptochrome and DNA photolyase, were also expressed at significantly higher levels in the light. Membrane transporters for Na+/phosphate and Na+/alanine symporters, and the Na+-translocating NADH-quinone oxidoreductase (NQR) linked electron transport chain, were also significantly upregulated in the light. Culture experiments using a specific inhibitor of Na+-translocating NQR indicated that sodium pumping via NQR is a critical metabolic process in the light-stimulated growth of MED134. In total, the results suggested the importance of both the PR-enabled, light-driven proton gradient, as well as the generation of a Na+ ion gradient, as essential components for light-enhanced growth in these flavobacteria.
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Acknowledgements
We thank Jarone Pinhassi for providing strain MED134 and Francis X (Buddy) Cunningham for providing MPTA. We are also grateful to Jamie W Becker for measuring DOC in media, Frank J Stewart for helping with the rRNA subtraction, Yanmei Shi for helping small RNA analyses and Rachel Barry for work in preparing samples for pyrosequencing. This work was supported by a grant from the Gordon and Betty Moore Foundation (EFD), the Office of Science (BER), US Department of Energy (EFD) and NSF Science and Technology Center Award EF0424599. This work is a contribution of the Center for Microbial Oceanography: Research and Education (C-MORE). H Kimura was supported by Postdoctoral Fellowships for Research Abroad of Japan Society for the Promotion of Science (JSPS).
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Kimura, H., Young, C., Martinez, A. et al. Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium. ISME J 5, 1641–1651 (2011). https://doi.org/10.1038/ismej.2011.36
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DOI: https://doi.org/10.1038/ismej.2011.36
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