Optimization of ATP Synthase c–Rings for Oxygenic Photosynthesis

Abstract

The conversion of sunlight into useable cellular energy occurs via the proton-coupled electron transfer reactions of photosynthesis. Light is absorbed by photosynthetic pigments and transferred to photochemical reaction centers to initiate electron and proton transfer reactions to store energy in a redox gradient and an electrochemical proton gradient (proton motive force, pmf), composed of a concentration gradient (DpH) and an electric field (Dy), which drives the synthesis of ATP through the thylakoid F o F 1 -ATP synthase. Although ATP synthase structure and function are conserved across biological kingdoms, the number of membrane-embedded ion-binding c subunits varies between organisms, ranging from 8 to 17, theoretically altering the H + /ATP ratio for different ATP synthase complexes, with profound implications for the bioenergetic processes of cellular metabolism. Of the known c-ring stoichiometries, photosynthetic c-rings are among the largest identified stoichiometries, and it has been proposed that decreasing the c-stoichiometry could increase the energy conversion efficiency of photosynthesis. Indeed, there is strong evidence that the high H + /ATP of the chloroplast ATP synthase results in a low ATP/nicotinamide adenine dinucleotide phosphate (NADPH) ratio produced by photosynthetic linear electron flow, requiring secondary processes such as cyclic electron flow to support downstream metabolism. We hypothesize that the larger c subunit stoichiometry observed in photosynthetic ATP synthases was selected for because it allows the thylakoid to maintain pmf in a range where ATP synthesis is supported, but avoids excess Dy and DpH, both of which can lead to production of reactive oxygen species and subsequent photodamage. Numerical kinetic simulations of the energetics of chloroplast photosynthetic reactions with altered cring size predicts the energy storage of pmf and its effects on the photochemical reaction centers strongly support this hypothesis, suggesting that, despite the low efficiency and suboptimal ATP/NADPH ratio, a high H + /ATP is favored to avoid photodamage. This has important implications for the evolution and regulation of photosynthesis as well as for synthetic biology efforts to alter photosynthetic efficiency by engineering the ATP synthase.

Here comes the sun: How optimization of photosynthetic light reactions can boost crop yields

“…Instead of indirectly upregulating the production of ATP through upregulation of CET routes, it is conceivable to directly enhance chloroplast ATP synthase activity (Cardona et al, 2018; Davis and Kramer, 2020). The ATP synthase is composed of two rotary motor complexes (CF0/CF1) which are connected by two flexible stalks (Kühlbrandt, 2019).…”

“…The ATP synthase is composed of two rotary motor complexes (CF0/CF1) which are connected by two flexible stalks (Kühlbrandt, 2019). The CF0 complex is embedded within the thylakoid membrane and consists of a ring of several c‐subunits, the numbers of which are organism/species‐dependent but remain constant under different conditions (between eight and 17 c‐subunits; Davis and Kramer, 2020). Each c‐subunit binds one proton from the thylakoid lumen, fueling the CF0 motor and subsequently the CF1 motor on the stromal side of the membrane, thus promoting the production of three ATP molecules per 360° rotation.…”

ATP synthase: Evolution, energetics, and membrane interactions

“…For instance, the large c-ring in B. pseudomallei has a high ion-to-ATP ratio, making the enzyme an efficient ion pump and allowing the pathogen to deal with the hostile acidic host phagosome ( Schulz et al, 2017 ). The overwhelming majority of studies have demonstrated that c-ring stoichiometries within a given species do not vary with external conditions like medium pH, host membrane composition, or carbon source ( Meier and Dimroth, 2002 ; Meyer zu Tittingdorf et al, 2004 ; Meier et al, 2005b , 2007 ; Fritz et al, 2008 ; Davis and Kramer, 2020 ; but see also, e.g., Schemidt et al, 1998 ). However, genetically engineered rotors of modified size have been shown to function in both “directions” within their host cell—that is, edited F1–Fo complexes can both synthesize and hydrolyze ATP.…”

Gloeobacter and the implications of a freshwater origin of Cyanobacteria

“…In Gloeobacter violaceus, the ATP synthase stoichiometry may be related to the occurrence of all membrane-associated bioenergetic processes in the cell membrane. Davis & Kramer (2020) suggest that the higher number of c-subunits in ATP synthases in photosynthetic membranes than in respiratory membranes is related to the use of a large pH difference component of a PMF). This seems more plausible for thylakoid membranes, when the P (lumen) side of the membrane has a relatively unconstrained pH, at least compared to the P (periplasmic) side of the membrane plasma membrane of Gloeobacter.…”