Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

ISME J. 2016 May;10(5):1102-12. doi: 10.1038/ismej.2015.196. Epub 2015 Nov 17.

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Flavobacteriaceae / genetics*
  • Flavobacteriaceae / metabolism*
  • Gene Expression Regulation, Bacterial
  • Light
  • Phylogeny
  • Rhodopsins, Microbial / metabolism
  • Seawater / microbiology
  • Thiamine / metabolism*
  • Vitamins / metabolism

Substances

  • Rhodopsins, Microbial
  • Vitamins
  • proteorhodopsin
  • Thiamine