Optimization of ATP synthase function in mitochondria and chloroplasts via the adenylate kinase equilibrium.

Abir U Igamberdiev,Leszek A Kleczkowski

doi:10.3389/fpls.2015.00010

Abir U Igamberdiev, Leszek A Kleczkowski

Open Access

https://doi.org/10.3389/fpls.2015.00010

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Abstract

The bulk of ATP synthesis in plants is performed by ATP synthase, the main bioenergetics engine of cells, operating both in mitochondria and in chloroplasts. The reaction mechanism of ATP synthase has been studied in detail for over half a century; however, its optimal performance depends also on the steady delivery of ATP synthase substrates and the removal of its products. For mitochondrial ATP synthase, we analyze here the provision of stable conditions for (i) the supply of ADP and Mg2+, supported by adenylate kinase (AK) equilibrium in the intermembrane space, (ii) the supply of phosphate via membrane transporter in symport with H+, and (iii) the conditions of outflow of ATP by adenylate transporter carrying out the exchange of free adenylates. We also show that, in chloroplasts, AK equilibrates adenylates and governs Mg2+ contents in the stroma, optimizing ATP synthase and Calvin cycle operation, and affecting the import of inorganic phosphate in exchange with triose phosphates. It is argued that chemiosmosis is not the sole component of ATP synthase performance, which also depends on AK-mediated equilibrium of adenylates and Mg2+, adenylate transport, and phosphate release and supply.

Highlights

ATP synthase is the central bioenergetic engine of all organisms and represents the smallest molecular motor, which was optimized in the course of evolution
The ATP synthase complex is located in the inner membrane of mitochondria, with ATP synthesis reaction occurring on the membrane side toward matrix compartment
ATP synthase receives protons from thylakoid lumen, which volume is small as compared to the mitochondrial intermembrane space (IMS) and which pH value can drop to the values below 5 (Oja et al, 1999), while in the mitochondrial IMS it drops only slightly below 7 (Moore and Rich, 1985; Porcelli et al, 2005)

Summary

INTRODUCTION

ATP synthase is the central bioenergetic engine of all organisms and represents the smallest molecular motor, which was optimized in the course of evolution. While generation of proton electrochemical potential became the central theory in the chemiosmotic concept of ATP synthase operation (Mitchell, 1961), the optimal conditions of delivery of ADP and phosphate were analyzed in the concept of thermodynamic buffering (Stucki, 1980a,b), underlying the importance of auxiliary buffering enzymes such as adenylate kinase (AK) and creatine kinase in provision of the stable flux of ADP to ATP synthase. This theory was extended in relation to operation of AK in the IMS of mitochondria (Igamberdiev and Kleczkowski, 2009). BUFFERING OF PROTONS BY OTHER CATIONS IN ATP SYNTHESIS According to the views of Mitchell (1961) and Williams (1961, 2011), the non-equilibrium hydrogen ion (proton) potentials are set up in biological phases by the electron transport chain (ETC)

Optimization of ATP synthase function

Findings

CONCLUSION