The evolution of A-, F-, and V-type ATP synthases and ATPases: reversals in function and changes in the H+/ATP coupling ratio.
Members of the FoF1, AoA1 and VoV1 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.
Cross
Richard L
RL
Department of Biochemistry and Molecular Biology, SUNY Upstate Medical University, Syracuse, NY 13210, USA. crossr@upstate.edu
Müller
Volker
V
D000251:Adenosine Triphosphatases / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism*; D000818:Animals; D001483:Base Sequence / Q000235:genetics; D020134:Catalytic Domain; D004926:Escherichia coli / Q000201:enzymology; D019143:Evolution, Molecular; D020440:Gene Duplication; D017506:H(+)-K(+)-Exchanging ATPase / Q000737:chemistry*; D006801:Humans; D008954:Models, Biological; D020836:Protein Structure, Quaternary; D006180:Proton-Translocating ATPases / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism*; D011522:Protons
D011522:Protons; D000251:Adenosine Triphosphatases; D017506:H(+)-K(+)-Exchanging ATPase; D006180:Proton-Translocating ATPases