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Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria

Nature Plants volume 3, Article number: 17089 (2017) | Download Citation

Abstract

The orange carotenoid protein (OCP) is a structurally and functionally modular photoactive protein involved in cyanobacterial photoprotection. Using phylogenomic analysis, we have revealed two new paralogous OCP families, each distributed among taxonomically diverse cyanobacterial genomes. Based on bioinformatic properties and phylogenetic relationships, we named the new families OCP2 and OCPx to distinguish them from the canonical OCP that has been well characterized in Synechocystis, denoted hereafter as OCP1. We report the first characterization of a carotenoprotein photoprotective system in the chromatically acclimating cyanobacterium Tolypothrix sp. PCC 7601, which encodes both OCP1 and OCP2 as well as the regulatory fluorescence recovery protein (FRP). OCP2 expression could only be detected in cultures grown under high irradiance, surpassing expression levels of OCP1, which appears to be constitutive; under low irradiance, OCP2 expression was only detectable in a Tolypothrix mutant lacking the RcaE photoreceptor required for complementary chromatic acclimation. In vitro studies show that Tolypothrix OCP1 is functionally equivalent to Synechocystis OCP1, including its regulation by Tolypothrix FRP, which we show is structurally similar to the dimeric form of Synechocystis FRP. In contrast, Tolypothrix OCP2 shows both faster photoconversion and faster back-conversion, lack of regulation by the FRP, a different oligomeric state (monomer compared to dimer for OCP1) and lower fluorescence quenching of the phycobilisome. Collectively, these findings support our hypothesis that the OCP2 is relatively primitive. The OCP2 is transcriptionally regulated and may have evolved to respond to distinct photoprotective needs under particular environmental conditions such as high irradiance of a particular light quality, whereas the OCP1 is constitutively expressed and is regulated at the post-translational level by FRP and/or oligomerization.

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Acknowledgements

This work was supported by the National Science Foundation (IOS 1557324). The authors thank W.F. Beck of Michigan State University for valuable discussions about the spectroscopic properties of carotenoids. The authors thank R. Burton for assistance in the DLS measurement. The Advanced Light Source is supported by the Director, Office of Science, Office of Basic Energy Sciences, of the US Department of Energy under Contract No. DE-AC02-05CH11231.

Author information

Affiliations

  1. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, USA

    • Han Bao
    • , Matthew R. Melnicki
    • , Emily G. Pawlowski
    • , Markus Sutter
    • , Marco Agostoni
    • , Sigal Lechno-Yossef
    • , Beronda L. Montgomery
    •  & Cheryl A. Kerfeld
  2. Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA

    • Matthew R. Melnicki
    • , Markus Sutter
    • , Fei Cai
    •  & Cheryl A. Kerfeld
  3. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824, USA

    • Beronda L. Montgomery
    •  & Cheryl A. Kerfeld
  4. Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48824, USA

    • Beronda L. Montgomery
  5. Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA

    • Cheryl A. Kerfeld

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Contributions

H.B. designed and performed the research, analysed and interpreted data, and wrote the article. C.A.K. designed the research, analysed and interpreted the data, and wrote the article. M.R.M. performed the bioinformatics and wrote the article. E.G.P., M.S., M.A., S.L.-Y., F.C. and B.L.M. performed the research and contributed to the analysis and interpretation of the data.

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The authors declare no competing financial interests.

Corresponding author

Correspondence to Cheryl A. Kerfeld.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1-8, Supplementary Tables 1-2, Supplementary References.

Excel files

  1. 1.

    Supplementary File 1

    Annotated gene and taxon IDs for OCPs, FRPs and cyanobacterial genomes used in bioinformatic analyses.

XML files

  1. 1.

    Supplementary File 2

    Phylogenetic tree of OCP sequences, with embedded metadata.

  2. 2.

    Supplementary File 3

    Phylogenetic tree of RpoC1 sequences, with embedded metadata.

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DOI

https://doi.org/10.1038/nplants.2017.89

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