Bicarbonate-induced redox tuning in Photosystem II for regulation and protection

Proc Natl Acad Sci U S A. 2016 Oct 25;113(43):12144-12149. doi: 10.1073/pnas.1608862113. Epub 2016 Oct 10.

Abstract

The midpoint potential (Em) of [Formula: see text], the one-electron acceptor quinone of Photosystem II (PSII), provides the thermodynamic reference for calibrating PSII bioenergetics. Uncertainty exists in the literature, with two values differing by ∼80 mV. Here, we have resolved this discrepancy by using spectroelectrochemistry on plant PSII-enriched membranes. Removal of bicarbonate (HCO3-) shifts the Em from ∼-145 mV to -70 mV. The higher values reported earlier are attributed to the loss of HCO3- during the titrations (pH 6.5, stirred under argon gassing). These findings mean that HCO3- binds less strongly when QA-• is present. Light-induced QA-• formation triggered HCO3- loss as manifest by the slowed electron transfer and the upshift in the Em of QA HCO3--depleted PSII also showed diminished light-induced 1O2 formation. This finding is consistent with a model in which the increase in the Em of [Formula: see text] promotes safe, direct [Formula: see text] charge recombination at the expense of the damaging back-reaction route that involves chlorophyll triplet-mediated 1O2 formation [Johnson GN, et al. (1995) Biochim Biophys Acta 1229:202-207]. These findings provide a redox tuning mechanism, in which the interdependence of the redox state of QA and the binding by HCO3- regulates and protects PSII. The potential for a sink (CO2) to source (PSII) feedback mechanism is discussed.

Keywords: CO2 fixation; photoassembly; photoinhibition; photosynthesis; water oxidation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bicarbonates / metabolism*
  • Carbon Cycle
  • Carbon Dioxide / chemistry
  • Carbon Dioxide / metabolism
  • Cell Membrane / chemistry
  • Cell Membrane / metabolism
  • Electron Transport
  • Hydrogen-Ion Concentration
  • Kinetics
  • Light
  • Oxidation-Reduction
  • Oxygen / chemistry
  • Oxygen / metabolism
  • Photosystem II Protein Complex / chemistry
  • Photosystem II Protein Complex / isolation & purification
  • Photosystem II Protein Complex / metabolism*
  • Plant Leaves / chemistry
  • Plant Leaves / metabolism
  • Plant Proteins / chemistry
  • Plant Proteins / isolation & purification
  • Plant Proteins / metabolism*
  • Quinones / chemistry
  • Quinones / metabolism*
  • Spinacia oleracea / chemistry
  • Spinacia oleracea / metabolism*
  • Superoxides / chemistry
  • Superoxides / metabolism
  • Thermodynamics

Substances

  • Bicarbonates
  • Photosystem II Protein Complex
  • Plant Proteins
  • Quinones
  • Superoxides
  • Carbon Dioxide
  • Oxygen