Unusual features of the c-ring of F1FO ATP synthases

Yu L Ryzhykau,V V Chupin,N A Dencher,I Yu Gushchin,V A Polovinkin,E S Round,A I Kuklin,G D Büldt,I S Okhrimenko,V I Borshchevskiy,S.-H Marx,V I Gordeliy,K V Kovalev,N M Tsoy,A V Rogachev,A V Vlasov

doi:10.1038/s41598-019-55092-z

Yu L Ryzhykau, V V Chupin + Show 14 more

Open Access

https://doi.org/10.1038/s41598-019-55092-z

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Abstract

Membrane integral ATP synthases produce adenosine triphosphate, the universal “energy currency” of most organisms. However, important details of proton driven energy conversion are still unknown. We present the first high-resolution structure (2.3 Å) of the in meso crystallized c-ring of 14 subunits from spinach chloroplasts. The structure reveals molecular mechanisms of intersubunit contacts in the c14-ring, and it shows additional electron densities inside the c-ring which form circles parallel to the membrane plane. Similar densities were found in all known high-resolution structures of c-rings of F1FO ATP synthases from archaea and bacteria to eukaryotes. The densities might originate from isoprenoid quinones (such as coenzyme Q in mitochondria and plastoquinone in chloroplasts) that is consistent with differential UV-Vis spectroscopy of the c-ring samples, unusually large distance between polar/apolar interfaces inside the c-ring and universality among different species. Although additional experiments are required to verify this hypothesis, coenzyme Q and its analogues known as electron carriers of bioenergetic chains may be universal cofactors of ATP synthases, stabilizing c-ring and prevent ion leakage through it.

Highlights

ATP synthases convert energy of H+ electrochemical gradient across the membrane into energy of chemical bonds in ATP molecules by coupling of H+ transfer and ATP synthesis
One more advance was the determination of the structure of the complete chloroplast ATP synthase from spinach by cryo–EM where all the 26 currently known protein subunits were resolved at a resolution of 2.9 Å to 3.4 Å6
We hypothesize that coenzyme Q and its analogues known as electron carriers of bioenergetics chains may be universal cofactors of ATP synthases and are necessary for stabilization of their FO rotary parts, prevention of ion leakage through the c14-ring and protection of the proton uptake/release center of c subunits against reactive oxygen species

Summary

Introduction

ATP synthases convert energy of H+ electrochemical gradient across the membrane into energy of chemical bonds in ATP molecules by coupling of H+ transfer and ATP synthesis. A remarkable feature of the structure is additional electron densities at 5.4 Å distance from each other inside the c-ring, which form circles, oriented parallel to membrane plane We demonstrate that such characteristic densities are present in all available high resolution structures of the c-rings[14,15,16,17,18,19]. We hypothesize that the densities originate from isoprenoid molecules (presumably quinone isoprenoids, such as coenzyme Q in mitochondria, plastoquinone in chloroplasts and menaquinone in bacteria) It is consistent with differential UV-Vis spectroscopy of the c-ring samples, unusually large distance between polar/apolar interfaces inside the c-ring and universality of the molecule among different organisms. We hypothesize that coenzyme Q and its analogues known as electron carriers of bioenergetics chains may be universal cofactors of ATP synthases and are necessary for stabilization of their FO rotary parts, prevention of ion leakage through the c14-ring and protection of the proton uptake/release center of c subunits against reactive oxygen species

Methods

Conclusion