title: Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria.
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-1(T), Dokdonia MED134 and Dokdonia PRO95, grown in identical seawater medium in light and darkness. Although only DSW-1(T) 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-1(T) 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-1(T) 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.
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA.
authors.forename: Laura
authors.initials: L
authors.lastname: Gómez-Consarnau
authors.affiliation: Department of Microbiology, University of La Laguna, La Laguna, Spain.
authors.forename: José M
authors.initials: JM
authors.lastname: González
authors.affiliation: Department of Microbial Ecology and Diversity Research, Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.
authors.forename: Thomas
authors.initials: T
authors.lastname: Riedel
authors.affiliation: Center for Biotechnology-CeBiTec, Bielefeld, Germany.
authors.forename: Sebastian
authors.initials: S
authors.lastname: Jaenicke
authors.affiliation: Research Group Microbial Communication, Helmholtz Centre for Infection Research, Braunschweig, Germany.
authors.forename: Irene
authors.initials: I
authors.lastname: Wagner-Döbler
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA.
authors.forename: Sergio A
authors.initials: SA
authors.lastname: Sañudo-Wilhelmy
authors.affiliation: Department of Biological Sciences, University of Southern California, Los Angeles, CA, USA.
authors.forename: Jed A
authors.initials: JA
authors.lastname: Fuhrman
mesh_terms: D041965:Flavobacteriaceae / Q000235:genetics* / Q000378:metabolism*; D015964:Gene Expression Regulation, Bacterial; D008027:Light; D010802:Phylogeny; D025604:Rhodopsins, Microbial / Q000378:metabolism; D012623:Seawater / Q000382:microbiology; D013831:Thiamine / Q000378:metabolism*; D014815:Vitamins / Q000378:metabolism
chemical_list: D025604:Rhodopsins, Microbial; D014815:Vitamins; C413548:proteorhodopsin; D013831:Thiamine