The photoactive orange carotenoid protein (OCP) is a blue-light intensity sensor involved in cyanobacterial photoprotection. Three OCP families co-exist (OCPX, OCP1 and OCP2), having originated from the fusion of ancestral domain genes. Here, we report the characterization of an OCPX and the evolutionary characterization of OCP paralogues focusing on the role of the linker connecting the domains. The addition of the linker with specific amino acids enabled the photocycle of the OCP ancestor. OCPX is the paralogue closest to this ancestor. A second diversification gave rise to OCP1 and OCP2. OCPX and OCP2 present fast deactivation and weak antenna interaction. In OCP1, OCP deactivation became slower and interaction with the antenna became stronger, requiring a further protein to detach OCP from the antenna and accelerate its deactivation. OCP2 lost the tendency to dimerize, unlike OCPX and OCP1, and the role of its linker is slightly different, giving less controlled photoactivation.
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The sequences of the OCPs isolated and studied in this article are accessible in the GenBank/EMBL data libraries (or the IMG database) under the following accession numbers: slr1963 (OCP1 Synechocystis, IMG ID: 2514153952), Fdi2450 (OCP1 Tolypothrix, IMG ID: 2501541336), Fdi7374 (OCP2 Tolypothrix, IMG ID: 2501546328) and WA1_RS11680 (OCPX Scytonema, IMG ID: 2551963320). The protein sequences and their corresponding identifiers for the IMG database used for the phylogenetic analysis can be found in the Supplementary Information (available as an .xls file in the online version of the article). The additional data that support the findings of this study are available from the corresponding author upon request.
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The authors thank S. Cot for technical help, F. Andre for helping with the phylogenetic analysis, L. Tabares for assisting with molecular dynamics simulations and M. Guillaume Sarrailhe for helping in the construction of the three OCP mutants. This work was supported by grants from the Agence Nationale de la Recherche (RECYFUEL project (grant no. ANR-16-CE05- 0026)) and from the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 675006 (SE2B)). F.M.’s salary was financed by the European Union’s Horizon 2020 (project no. SE2B). The research was also supported by the Centre National de la Recherche Scientifique and the Commissariat à l’Energie Atomique. The French Infrastructure for Integrated Structural Biology (grant no. ANR-10-INBS-05) also partially supported this research.
The authors declare no competing interests.
Peer review information Nature Plants thanks Roberto Bassi and Conrad Mullineaux and other, anonymous, reviewers for their contribution to the peer review of this work.
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Muzzopappa, F., Wilson, A. & Kirilovsky, D. Interdomain interactions reveal the molecular evolution of the orange carotenoid protein. Nat. Plants 5, 1076–1086 (2019). https://doi.org/10.1038/s41477-019-0514-9
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