Cyanobacterial Light-Driven Proton Pump, Gloeobacter Rhodopsin: Complementarity Between Rhodopsin-Based Energy Production and Photosynthesis

PLoS One. 2014 Oct 27;9(10):e110643. doi: 10.1371/journal.pone.0110643. eCollection 2014.

Abstract

A homologue of type I rhodopsin was found in the unicellular Gloeobacter violaceus PCC7421, which is believed to be primitive because of the lack of thylakoids and peculiar morphology of phycobilisomes. The Gloeobacter rhodopsin (GR) gene encodes a polypeptide of 298 amino acids. This gene is localized alone in the genome unlike cyanobacterium Anabaena opsin, which is clustered together with 14 kDa transducer gene. Amino acid sequence comparison of GR with other type I rhodopsin shows several conserved residues important for retinal binding and H+ pumping. In this study, the gene was expressed in Escherichia coli and bound all-trans retinal to form a pigment (λmax = 544 nm at pH 7). The pKa of proton acceptor (Asp121) for the Schiff base, is approximately 5.9, so GR can translocate H+ under physiological conditions (pH 7.4). In order to prove the functional activity in the cell, pumping activity was measured in the sphaeroplast membranes of E. coli and one of Gloeobacter whole cell. The efficient proton pumping and rapid photocycle of GR strongly suggests that Gloeobacter rhodopsin functions as a proton pumping in its natural environment, probably compensating the shortage of energy generated by chlorophyll-based photosynthesis without thylakoids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Biological Transport
  • Cyanobacteria / classification
  • Cyanobacteria / genetics*
  • Cyanobacteria / metabolism*
  • Energy Metabolism*
  • Gene Expression
  • Light
  • Molecular Sequence Data
  • Mutation
  • Photosynthesis*
  • Phylogeny
  • Proton Pumps / genetics*
  • Proton Pumps / metabolism
  • Protons
  • Rhodopsin / genetics*
  • Rhodopsin / metabolism

Substances

  • Proton Pumps
  • Protons
  • Rhodopsin

Grant support

This work was supported by grants from the Research Foundation of Korea (2011-0012320 and 2011-220-C00057) and National Nuclear R& D Program funded by the Ministry of Science ICT & future planning (2012055325) to K.H. Jung, and grants from NSERC and PREA to L.S. Brown. A.R. Choi was supported by NRF-2013R1A1A064883. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.