Functional Characterization of Flavobacteria Rhodopsins Reveals a Unique Class of Light-Driven Chloride Pump in Bacteria

Proc Natl Acad Sci U S A. 2014 May 6;111(18):6732-7. doi: 10.1073/pnas.1403051111. Epub 2014 Mar 31.

Abstract

Light-activated, ion-pumping rhodopsins are broadly distributed among many different bacteria and archaea inhabiting the photic zone of aquatic environments. Bacterial proton- or sodium-translocating rhodopsins can convert light energy into a chemiosmotic force that can be converted into cellular biochemical energy, and thus represent a widespread alternative form of photoheterotrophy. Here we report that the genome of the marine flavobacterium Nonlabens marinus S1-08(T) encodes three different types of rhodopsins: Nonlabens marinus rhodopsin 1 (NM-R1), Nonlabens marinus rhodopsin 2 (NM-R2), and Nonlabens marinus rhodopsin 3 (NM-R3). Our functional analysis demonstrated that NM-R1 and NM-R2 are light-driven outward-translocating H(+) and Na(+) pumps, respectively. Functional analyses further revealed that the light-activated NM-R3 rhodopsin pumps Cl(-) ions into the cell, representing the first chloride-pumping rhodopsin uncovered in a marine bacterium. Phylogenetic analysis revealed that NM-R3 belongs to a distinct phylogenetic lineage quite distant from archaeal inward Cl(-)-pumping rhodopsins like halorhodopsin, suggesting that different types of chloride-pumping rhodopsins have evolved independently within marine bacterial lineages. Taken together, our data suggest that similar to haloarchaea, a considerable variety of rhodopsin types with different ion specificities have evolved in marine bacteria, with individual marine strains containing as many as three functionally different rhodopsins.

Keywords: ecology; evolution; photoheterotroph; photoproteins; retinal.

Publication types

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

MeSH terms

  • Chlorides / metabolism*
  • Evolution, Molecular
  • Flavobacteriaceae / genetics
  • Flavobacteriaceae / metabolism*
  • Flavobacteriaceae / radiation effects
  • Genome, Bacterial
  • Ion Pumps / classification*
  • Ion Pumps / genetics
  • Ion Pumps / radiation effects
  • Light
  • Molecular Sequence Data
  • Phylogeny
  • Rhodopsin / genetics
  • Rhodopsin / metabolism*

Substances

  • Chlorides
  • Ion Pumps
  • Rhodopsin

Associated data

  • GENBANK/AP014548
  • GENBANK/BAO54106
  • GENBANK/BAO54132
  • GENBANK/BAO54171
  • GENBANK/BAO54172
  • GENBANK/BAO55276