Paralogs of the C-Terminal Domain of the Cyanobacterial Orange Carotenoid Protein Are Carotenoid Donors to Helical Carotenoid Proteins

Plant Physiol. 2017 Nov;175(3):1283-1303. doi: 10.1104/pp.17.01040. Epub 2017 Sep 21.

Abstract

The photoactive Orange Carotenoid Protein (OCP) photoprotects cyanobacteria cells by quenching singlet oxygen and excess excitation energy. Its N-terminal domain is the active part of the protein, and the C-terminal domain regulates the activity. Recently, the characteristics of a family of soluble carotenoid-binding proteins (Helical Carotenoid Proteins [HCPs]), paralogs of the N-terminal domain of OCP, were described. Bioinformatics studies also revealed the existence of genes coding for homologs of CTD. Here, we show that the latter genes encode carotenoid proteins (CTDHs). This family of proteins contains two subgroups with distinct characteristics. One CTDH of each clade was further characterized, and they proved to be very good singlet oxygen quenchers. When synthesized in Escherichia coli or Synechocystis PCC 6803, CTDHs formed dimers that share a carotenoid molecule and are able to transfer their carotenoid to apo-HCPs and apo-OCP. The CTDHs from clade 2 have a cysteine in position 103. A disulfide bond is easily formed between the monomers of the dimer preventing carotenoid transfer. This suggests that the transfer of the carotenoid could be redox regulated in clade 2 CTDH. We also demonstrate here that apo-OCPs and apo-CTDHs are able to take the carotenoid directly from membranes, while HCPs are unable to do so. HCPs need the presence of CTDH to become holo-proteins. We propose that, in cyanobacteria, the CTDHs are carotenoid donors to HCPs.

MeSH terms

  • Amino Acid Sequence
  • Apoproteins / chemistry
  • Apoproteins / metabolism
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism*
  • Canthaxanthin / metabolism
  • Carotenoids / metabolism*
  • Consensus Sequence
  • Escherichia coli / metabolism
  • Evolution, Molecular
  • Fluorescence
  • Models, Biological
  • Models, Molecular
  • Phylogeny
  • Protein Binding
  • Protein Domains
  • Protein Multimerization
  • Sequence Homology, Amino Acid*
  • Spectrum Analysis
  • Synechocystis / metabolism*

Substances

  • Apoproteins
  • Bacterial Proteins
  • orange carotenoid protein, Synechocystis
  • Carotenoids
  • Canthaxanthin