title: Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium.
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.
authors.affiliation: Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Kimura
authors.forename: Curtis R
authors.initials: CR
authors.lastname: Young
authors.forename: Asuncion
authors.initials: A
authors.lastname: Martinez
authors.forename: Edward F
authors.initials: EF
authors.lastname: Delong
mesh_terms: D001426:Bacterial Proteins / Q000378:metabolism; D002352:Carrier Proteins / Q000378:metabolism; D004579:Electron Transport; D005417:Flavobacterium / Q000235:genetics* / Q000254:growth & development* / Q000378:metabolism; D008027:Light; D011808:Quinone Reductases / Q000378:metabolism; D012243:Rhodopsin / Q000378:metabolism*; D025604:Rhodopsins, Microbial; D050608:Sodium-Phosphate Cotransporter Proteins / Q000378:metabolism; D014158:Transcription, Genetic
chemical_list: D001426:Bacterial Proteins; D002352:Carrier Proteins; D025604:Rhodopsins, Microbial; D050608:Sodium-Phosphate Cotransporter Proteins; C413548:proteorhodopsin; D012243:Rhodopsin; C041831:NADH dehydrogenase (quinone); D011808:Quinone Reductases