Evolution and Structural and Functional Modularity of the Cyanobacterial Orange Carotenoid Protein

Cheryl A. Kerfeld
DOE-MSU Plant Research Lab and Department of Biochemistry and Molecular Biology, Michigan State University and Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Plant and Microbial Biology University of California, Berkeley, Berkeley California, USA

In contrast to those of plants, the photoprotective mechanisms of cyanobacteria have only recently begun to be characterized. One of the most prevalent, the OCP/FRP (Orange Carotenoid Protein/Fluorescence Recovery Protein) system responds to high light by converting from an orange, resting form of the protein OCPO, to a red, active, quenching form, OCPR. The crystal structure of the OCPO[1] shows that the protein is comprised of two structural domains: an all-helical N-terminal domain (NTD), unique to cyanobacteria, and a C-terminal domain (CTD) that provides the only hydrogen bonds to the single associated carotenoid. The OCP’s structural modularity extends to function [2]. In the absence of the CTD, the NTD of the OCP retains the carotenoid and is constitutively active. The CTD appears to regulate the function of the NTD by priming carotenoid photochemistry in OCPO and by acting as a substrate for FRP. Structural studies demonstrated that the NTD and CTD of the OCP fully dissociate in the conversion from OCPO to OCPR [3], a prerequisite for quenching.

Biophysical and structural studies of the NTD with bound carotenoid and of the OCPR reveal that the carotenoid occupies a distinctly different position in these active forms relative to that in OCPO[4]. The carotenoid-protein configuration of the activated form of the protein is defined by unique carotenoid-NTD interactions resulting from a 12 Å translocation of the carotenoid that effectively buries its polyene chain entirely within the NTD.

Newly available genomic sequence data from non-model, ecophysiologically diverse cyanobacteria indicate that many cyanobacteria, especially those occupying dynamic environments, contain multiple copies of genes for homologs of the NTD [5]. We have shown that these NTD homologs bind carotenoids, are likely functionally diverse, and provide insight into the evolution of the OCP.

References

[1] C.A. Kerfeld et al., Structure 2003, 11, 55-65; A. Wilson et al., JBC 2010, 285,18364-18375.
[2] R.L. Leverenz et al, Plant Cell 2014, 26, 426-437.
[3] S. Gupta, et al. PNAS 2015, 112, E5567-5574.
[4] R.L. Leverenz et al. Science 2015, 348, 1463-1466.
[5] M.R. Melnicki et al., Molecular Plant in revision.