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 o F 1 , A o A 1 and V o V 1 family of ATP synthases and ATPases have undergone at least two reversals in primary function. The first was from a progenitor protonpumping 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 þ /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 nucleotidebinding catalytic subunits followed by loss of function in one of the genes. The halving of the ratio that occurred at the Synthaseto-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 finetuning of the H þ /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.

Niche adaptation and genome expansion in the chlorophyll d -producing cyanobacterium Acaryochloris marina

“…These genes are arranged into a unique operon and the individual proteins do not clearly fit into any of the described families (SI Fig. 5) (25). This unusual operon is conserved with full synteny in a remarkable array of organisms, including cyanobacteria, archaea, planctomycetes, chlorobi, and proteobacteria (SI Fig.…”

Power Stroke Angular Velocity Profiles of Archaeal A-ATP Synthase Versus Thermophilic and Mesophilic F-ATP Synthase Molecular Motors

“…Both motors are connected by two peripheral stalks each composed of an EH heterodimer. These complexes share common features with bacterial F 1 F O -ATP synthases (F 1 , ␣ 3 ␤ 3 ␥␦⑀; and F O , ab 2 c 9 -15 ) and V 1 V O -ATPases (V 1 , A 3 B 3 CDE 3 FG 3 H; and V O , ac X cЈ Y cЉ Z de) (3)(4)(5)(6). In each case, the motors are connected by a central stalk that serves as an axle, as well as by one (F-ATP synthases) or three (V-ATPases) peripheral stalks.…”

“…Metabolism in archaea is coupled to the generation of H ϩ and/or Na ϩ potentials across the membrane, both of which can provide the energy for ATP synthesis by the A 1 A O -ATP synthase. Whereas the F 1 F O -ATP synthases in prokaryotes and eukaryotes catalyze ATP synthesis at the expense of an electrochemical ion potential, the evolutionarily related V 1 V O -ATPases function as ATP-driven ion pumps and are unable to synthesize ATP under physiological conditions (3)(4)(5). Although the cellular function of archaeal ATP synthases is to synthesize ATP powered by a non-equilibrium electrochemical gradient, they also work as ATP-driven ion pumps to generate an ion gradient under fermentative conditions (6).…”

Biophysical comparison of ATP synthesis mechanisms shows a kinetic advantage for the rotary process

“…It spurred Mitchell's chemiosmotic hypothesis (1) and Boyer's now-validated proposal for the binding-change mechanism (2) in which a proton electrochemical gradient is transduced to rotationbased mechanical energy and then back to chemical FE as ADP is phosphorylated. The F-ATPase's two-domain uniaxial rotary structure is conserved across all three domains of life (3)(4)(5)(6), and details of its function have been the subject of a multitude of studies (e.g., refs. .…”