The evolution of A-, F-, and V-type ATP synthases and ATPases: reversals in function and changes in the H⁺/ATP coupling ratio

Abstract 

Members of the F_oF₁, A_oA₁ and V_oV₁ family of ATP synthases and ATPases have undergone at least two reversals in primary function. The first was from a progenitor proton-pumping ATPase to a proton-driven ATP synthase. The second involved transforming the synthase back into a proton-pumping ATPase. As proposed earlier [FEBS Lett. 259 (1990) 227], these reversals required changes in the H⁺/ATP coupling ratio from an optimal value of about 2 for an ATPase function to about 4 for an ATP synthase function. The doubling of the ratio that occurred at the ATPase-to-Synthase transition was accomplished by duplicating the gene that encodes the nucleotide-binding catalytic subunits followed by loss of function in one of the genes. The halving of the ratio that occurred at the Synthase-to-ATPase transition was achieved by a duplication/fusion of the gene that encodes the proton-binding transporter subunits, followed by a loss of function in one half of the double-sized protein. These events allowed conservation of quaternary structure, while maintaining a sufficient driving force to sustain an adequate phosphorylation potential or electrochemical gradient. Here, we describe intermediate evolutionary steps and a fine-tuning of the H⁺/ATP coupling ratio to optimize synthase function in response to different environments. In addition, we propose a third reversal of function, from an ATPase back to an ATP synthase. In contrast to the first two reversals which required a partial loss in function, the change in coupling ratio required for the third reversal is explained by a gain in function.

Abbreviations:  The sources of ATP synthases and ATPases are denoted as A_oA₁ for archaea, F_oF₁ for bacteria MF_oF₁ for mitochondria CF_oF₁ for chloroplasts, V_oV₁ for vacuolar membranes

Keywords:  A_oA₁, F_oF₁, V_oV₁, ATP synthase, ATPase