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The Oligomeric State of c Rings from Cyanobacterial F-ATP Synthases Varies from 13 to 15

Denys Pogoryelov,^1,2, Christian Reichen,^1, Adriana L. Klyszejko,³ René Brunisholz,⁴ Daniel J. Muller,³ Peter Dimroth,^1* and Thomas Meier^2*

Institute of Microbiology, Eidgenössische Technische Hochschule (ETH) Zurich, Wolfgang-Pauli-Str. 10, CH-8093 Zurich, Switzerland,¹ Max-Planck-Institute of Biophysics, Max-von-Laue-Str. 3, 60438 Frankfurt am Main, Germany,² Center for Biotechnology, University of Technology, Tatzberg 49, 01307 Dresden, Germany,³ Functional Genomics Center Zurich, University of Zurich and ETH, Winterthurerstrasse 190, 8057 Zurich, Switzerland⁴

Received 16 April 2007/ Accepted 22 May 2007

We isolated the c rings of F-ATP synthases from eight cyanobacterial strains belonging to four different taxonomic classes (Chroococcales, Nostocales, Oscillatoriales, and Gloeobacteria). These c rings showed different mobilities on sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE), probably reflecting their molecular masses. This supposition was validated with the previously characterized c₁₁, c₁₄, and c₁₅ rings, which migrated on SDS-PAGE in proportion to their molecular masses. Hence, the masses of the cyanobacterial c rings can conveniently be deduced from their electrophoretic mobilities and, together with the masses of the c monomers, allow the calculation of the c ring stoichiometries. The method is a simple and fast way to determine stoichiometries of SDS-stable c rings and hence a convenient means to unambiguously determine the ion-to-ATP ratio, a parameter reflecting the bioenergetic efficacy of F-ATP synthases. AFM imaging was used to prove the accuracy of the method and confirmed that the c ring of Synechococcus elongatus SAG 89.79 is a tridecameric oligomer. Despite the high conservation of the c-subunit sequences from cyanobacterial strains from various environmental groups, the stoichiometries of their c rings varied between c₁₃ and c₁₅. This systematic study of the c-ring stoichiometries suggests that variability of c-ring sizes might represent an adaptation of the individual cyanobacterial species to their particular environmental and physiological conditions. Furthermore, the two new examples of c₁₅ rings underline once more that an F₁/F_o symmetry mismatch is not an obligatory feature of all F-ATP synthases.

Published ahead of print on 1 June 2007.

D. Pogoryelov and C. Reichen contributed equally to this paper.

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