title: Natural isoforms of the Photosystem II D1 subunit differ in photoassembly efficiency of the water-oxidizing complex.
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 (Mn(2+), Ca(2+), 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 Mn(3+) 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.
authors.affiliation: Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, 190 Frelinghuysen Rd., Piscataway, NJ, 08854, USA.|Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, NJ, 08854, USA.|Department of Chemistry, Yale University, New Haven, CT, 06520, USA.
authors.forename: David J
authors.initials: DJ
authors.lastname: Vinyard
authors.affiliation: Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, 190 Frelinghuysen Rd., Piscataway, NJ, 08854, USA.|Department of Molecular, Cellular, and Development Biology, Yale University, New Haven, CT, 06520, USA.
authors.forename: Jennifer S
authors.initials: JS
authors.lastname: Sun
authors.affiliation: San Diego Center for Algae Biotechnology, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, 92093, USA.|Centre for Biotechnology and Bioengineering, Universidad de Chile, Santiago, Chile.
authors.forename: Javier
authors.initials: J
authors.lastname: Gimpel
authors.affiliation: Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, 190 Frelinghuysen Rd., Piscataway, NJ, 08854, USA.|Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, NJ, 08854, USA.
authors.forename: Gennady M
authors.initials: GM
authors.lastname: Ananyev
authors.affiliation: San Diego Center for Algae Biotechnology, Division of Biological Sciences, University of California, San Diego, La Jolla, CA, 92093, USA.
authors.forename: Stephen P
authors.initials: SP
authors.lastname: Mayfield
authors.affiliation: Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, 190 Frelinghuysen Rd., Piscataway, NJ, 08854, USA. dismukes@rci.rutgers.edu.|Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, NJ, 08854, USA. dismukes@rci.rutgers.edu.
authors.forename: G
authors.identifier: http://orcid.org/0000-0003-0155-0541
authors.initials: G
authors.lastname: Charles Dismukes
mesh_terms: D016825:Chlamydomonas reinhardtii / Q000502:physiology* / Q000528:radiation effects; D008027:Light; D010084:Oxidation-Reduction; D010100:Oxygen / Q000378:metabolism*; D010788:Photosynthesis / Q000528:radiation effects*; D045332:Photosystem II Protein Complex / Q000378:metabolism* / Q000528:radiation effects; D020033:Protein Isoforms; D014867:Water / Q000378:metabolism*
chemical_list: D045332:Photosystem II Protein Complex; D020033:Protein Isoforms; D014867:Water; D010100:Oxygen
keywords: Oxygen evolution; Photo-assembly; Photosynthetic efficiency; Photosystem II; Water-oxidizing complex