Abstract
In photosynthesis, cyanobacteria, algae and plants fix carbon dioxide (CO2) into carbohydrates; this is necessary to support life on Earth. Over 50years ago, Otto Heinrich Warburg discovered a unique stimulatory role of CO2 in the Hill reaction (i.e., O2 evolution accompanied by reduction of an artificial electron acceptor), which, obviously, does not include any carbon fixation pathway; Warburg used this discovery to support his idea that O2 in photosynthesis originates in CO2. During the 1960s, a large number of researchers attempted to decipher this unique phenomenon, with limited success. In the 1970s, Alan Stemler, in Govindjee's lab, perfected methods to get highly reproducible results, and observed, among other things, that the turnover of Photosystem II (PSII) was stimulated by bicarbonate ions (hydrogen carbonate): the effect would be on the donor or the acceptor, or both sides of PSII. In 1975, Thomas Wydrzynski, also in Govindjee's lab, discovered that there was a definite bicarbonate effect on the electron acceptor (the plastoquinone) side of PSII. The most recent 1.9Å crystal structure of PSII, unequivocally shows HCO3− bound to the non-heme iron that sits in-between the bound primary quinone electron acceptor, QA, and the secondary quinone electron acceptor QB. In this review, we focus on the historical development of our understanding of this unique bicarbonate effect on the electron acceptor side of PSII, and its mechanism as obtained by biochemical, biophysical and molecular biological approaches in many laboratories around the World. We suggest an atomic level model in which HCO3−/CO32− plays a key role in the protonation of the reduced QB. In addition, we make comments on the role of bicarbonate on the donor side of PSII, as has been extensively studied in the labs of Alan Stemler (USA) and Vyacheslav Klimov (Russia). We end this review by discussing the uniqueness of bicarbonate's role in oxygenic photosynthesis and its role in the evolutionary development of O2-evolving PSII. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: from Natural to Artificial.
► Location and function of bicarbonate in photosynthesis is reviewed. ► Bicarbonate is required for Photosystem II, not for Photosystem I reactions. ► Bicarbonate is bound to the non-heme iron on the acceptor side of Photosystem II. ► Bicarbonate functions in protonation at the “two-electron gate” of Photosystem II. ► Mechanism of bicarbonate-mediated QB protonation is discussed.