Photosystem II (PSII) contains a non-heme ferrous ion, located on the stromal side of the protein in close proximity to quinones A and B (Q(A) and Q(B)). We used EPR spectroscopy to examine the temperature-dependent redox reactions of the iron-quinone site, using it as a probe of potentially physiologically relevant proton-coupled electron-transfer (PCET) reactions. Complete chemical oxidation of the non-heme iron at ambient temperatures was followed by cryogenic photoreduction, producing a temperature-dependent yield of Fe(2+)Q(A) (or Fe(3+)Q(A)(-))...Chl(+)/Car(+)/Y(D)(*) charge separations. These charge separations were subsequently observed to partially recombine in the dark at cryogenic temperatures. We observed no double photochemical charge separations upon illumination at temperatures <or=30 K, demonstrating that Q(A) and Fe(3+) together act as a single electron-accepting moiety at very low temperatures. Our results indicate the existence of two populations of the iron-quinone site in PSII, one whose Fe(3+) signal is abolished by illumination at liquid helium temperatures and one whose Fe(3+) signal is abolished by illumination only above 75 K. The observation of non-heme iron photoreduction at cryogenic temperatures (possibly at liquid helium temperatures and certainly above 75 K) implies the existence of a low reorganization energy proton-transfer (ET) pathway within the protein to the non-heme iron environment, of possible relevance to the PCET reactions of Q(B) and/or the non-heme iron itself. Furthermore, we observed the partial reoxidation of the non-heme iron by charge recombination with previously oxidized chlorophyll, carotenoid, and Y(D) within PSII. This electron transfer might be important in the photoprotective transfer of oxidative power away from P(680)(+) and the oxygen-evolving complex in stressed PSII centers.