Twisting a β-Carotene, an Adaptive Trick from Nature for Dissipating Energy during Photoprotection

J Biol Chem. 2017 Jan 27;292(4):1396-1403. doi: 10.1074/jbc.M116.753723. Epub 2016 Dec 19.

Abstract

Cyanobacteria possess a family of one-helix high light-inducible proteins (Hlips) that are homologous to light-harvesting antenna of plants and algae. An Hlip protein, high light-inducible protein D (HliD) purified as a small complex with the Ycf39 protein is evaluated using resonance Raman spectroscopy. We show that the HliD binds two different β-carotenes, each present in two non-equivalent binding pockets with different conformations, having their (0,0) absorption maxima at 489 and 522 nm, respectively. Both populations of β-carotene molecules were in all-trans configuration and the absorption position of the farthest blue-shifted β-carotene was attributed entirely to the polarizability of the environment in its binding pocket. In contrast, the absorption maximum of the red-shifted β-carotene was attributed to two different factors: the polarizability of the environment in its binding pocket and, more importantly, to the conformation of its β-rings. This second β-carotene has highly twisted β-rings adopting a flat conformation, which implies that the effective conjugation length N is extended up to 10.5 modifying the energetic levels. This increase in N will also result in a lower S1 energy state, which may provide a permanent energy dissipation channel. Analysis of the carbonyl stretching region for chlorophyll a excitations indicates that the HliD binds six chlorophyll a molecules in five non-equivalent binding sites, with at least one chlorophyll a presenting a slight distortion to its macrocycle. The binding modes and conformations of HliD-bound pigments are discussed with respect to the known structures of LHCII and CP29.

Keywords: carotenoid; chlorophyll; cyanobacteria; light-harvesting complex (antenna complex); photosynthesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Light-Harvesting Protein Complexes / chemistry*
  • Light-Harvesting Protein Complexes / genetics
  • Protein Domains
  • Protein Structure, Quaternary
  • Protein Structure, Secondary
  • Synechocystis / chemistry*
  • Synechocystis / genetics
  • beta Carotene / chemistry*
  • beta Carotene / genetics

Substances

  • Bacterial Proteins
  • Light-Harvesting Protein Complexes
  • beta Carotene