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Natural isoforms of the Photosystem II D1 subunit differ in photoassembly efficiency of the water-oxidizing complex

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Abstract

Oxygenic photosynthesis efficiency at increasing solar flux is limited by light-induced damage (photoinhibition) of Photosystem II (PSII), primarily targeting the D1 reaction center subunit. Some cyanobacteria contain two natural isoforms of D1 that function better under low light (D1:1) or high light (D1:2). Herein, rates and yields of photoassembly of the Mn4CaO5 water-oxidizing complex (WOC) from the free inorganic cofactors (Mn2+, Ca2+, water, electron acceptor) and apo-WOC-PSII are shown to differ significantly: D1:1 apo-WOC-PSII exhibits a 2.3-fold faster rate-limiting step of photoassembly and up to seven-fold faster rate to the first light-stable Mn3+ intermediate, IM1*, but with a much higher rate of photoinhibition than D1:2. Conversely, D1:2 apo-WOC-PSII assembles slower but has up to seven-fold higher yield, achieved by a higher quantum yield of charge separation and slower photoinhibition rate. These results confirm and extend previous observations of the two holoenzymes: D1:2-PSII has a greater quantum yield of primary charge separation, faster [P680 + Q −A ] charge recombination and less photoinhibition that results in a slower rate and higher yield of photoassembly of its apo-WOC-PSII complex. In contrast, D1:1-PSII has a lower quantum yield of primary charge separation, a slower [P680 + Q −A ] charge recombination rate, and faster photoinhibition that together result in higher rate but lower yield of photoassembly at higher light intensities. Cyanobacterial PSII reaction centers that contain the high- and low-light D1 isoforms can tailor performance to optimize photosynthesis at varying light conditions, with similar consequences on their photoassembly kinetics and yield. These different efficiencies of photoassembly versus photoinhibition impose differential costs for biosynthesis as a function of light intensity.

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Acknowledgments

This work was supported by grants from the National Science Foundation-Chemistry of Life Processes, CHE1213772 (to GCD), and the U.S. Department of Energy, Consortium for Algal Biofuels Commercialization, Grant DE-EE0003373 (to SPM). JSS was supported by the Waksman Institute of Microbiology and the Aresty Research Center for Undergraduates at Rutgers University. DJV was supported by the Department of Deference Army Research Office through a National Defense Science and Engineering Graduate (NDSEG - 32CFR168a), and a National Science Foundation Graduate Research Fellowship, DGE-0937373. JG was supported by the Comisión Nacional de Investigación Científica y Tecnológica de Chile (CONICYT). We thank Clyde Cady for assistance with EPR measurements.

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  1. David J. Vinyard

    Present address: Department of Chemistry, Yale University, New Haven, CT, 06520, USA

  2. Jennifer S. Sun

    Present address: Department of Molecular, Cellular, and Development Biology, Yale University, New Haven, CT, 06520, USA

  3. Javier Gimpel

    Present address: Centre for Biotechnology and Bioengineering, Universidad de Chile, Santiago, Chile

Authors and Affiliations

  1. Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, 190 Frelinghuysen Rd., Piscataway, NJ, 08854, USA

    David J. Vinyard, Jennifer S. Sun, Gennady M. Ananyev & G. Charles Dismukes

  2. Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, NJ, 08854, USA

    David J. Vinyard, Gennady M. Ananyev & G. Charles Dismukes

  3. San Diego Center for Algae Biotechnology, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, 92093, USA

    Javier Gimpel & Stephen P. Mayfield

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  1. David J. Vinyard
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Correspondence to G. Charles Dismukes.

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Vinyard, D.J., Sun, J.S., Gimpel, J. et al. Natural isoforms of the Photosystem II D1 subunit differ in photoassembly efficiency of the water-oxidizing complex. Photosynth Res 128, 141–150 (2016). https://doi.org/10.1007/s11120-015-0208-8

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  • DOI: https://doi.org/10.1007/s11120-015-0208-8

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