Structure-function correlations and system dynamics in oxygenic photosynthesis: classical perspectives and murburn precepts

Abstract

In this first part of our essay on oxygenic photosynthesis, we address the various aspects of classical and murburn explanations. We had recently pointed out that the classical explanations of- trans-membrane potential (TMP)-based chemiosmotic rotary ATP synthesis, quinone-cycle at cytochrome b 6 f, chartered electron transport by plastocyanin, and modality of light’s interaction with chloroplast pigments- are untenable. In lieu, we proposed a diffusible reactive (oxygen) species (DROS)-based murburn model. In continuum, herein, we assess the operational viability of the cyclic oxygenesis and electron transport chain (ETC) explanations for oxygenic photosynthesis, in the light of updated structural/mechanistic information. Further, thermodynamically validated murburn equations of photolysis-photophosphorylation (Pl-Pp) are provided, along with the rationale for organelle-homeostasis. We propose that the photo-excitation of various pigments leads to the formation of aquated electrons (eaq) and DROS in milieu, which are stabilized by a pool of redox-active elements within chloroplasts. Subsequently, the ‘eaq+DR(O)S’ pool is utilized stochastically via disordered/parallel reactions at the stacked thylakoid membrane interface. Effective charge separation by ‘photosystem switches’ enables delocalized oxygenesis, NAD(P) reduction and ADP phosphorylation. Heat/TMP/DROS generation is also an outcome of this process. Finally, we compare the murburn and classical models of Pl-Pp and delineate agendas for their ratification/falsification. Communicated by Ramaswamy H. Sarma Highlights Contemporary beliefs on oxygenic photosynthesis are critiqued. Murburn model is suggested as an alternative explanation. In the new model, diffusible reactive species are the main protagonists. All pigments are deemed photo-redox active in the new stochastic mechanism. NADPH synthesis occurs via simple electron transfers, not via elaborate ETC. Oxygenesis is delocalized and not just centered at Mn-Complex. Energetics of murburn proposal for photophosphorylation is provided. The proposal ushers in a paradigm shift in photosynthesis research.