A New Type of Proton Coordination in an F1Fo-ATP Synthase Rotor Ring
Laura Preiss1, Özkan Yildiz1, David B. Hicks2, Terry A. Krulwich2, Thomas Meier1,3*
1 Department of Structural Biology, Max-Planck Institute of Biophysics, Frankfurt, Germany, 2 Department of Pharmacology and Systems Therapeutics, Mount Sinai School of Medicine, New York, New York, United States of America, 3 Cluster of Excellence Macromolecular Complexes, Max-Planck Institute of Biophysics, Frankfurt, Germany
Source/Fonte: Medical Research Council - Mitochondrial Biology Unit
Abstract
We solved the crystal structure of a novel type of c-ring isolated from Bacillus pseudofirmus OF4 at 2.5 Å, revealing a cylinder with a tridecameric stoichiometry, a central pore, and an overall shape that is distinct from those reported thus far. Within the groove of two neighboring c-subunits, the conserved glutamate of the outer helix shares the proton with a bound water molecule which itself is coordinated by three other amino acids of outer helices. Although none of the inner helices contributes to ion binding and the glutamate has no other hydrogen bonding partner than the water oxygen, the site remains in a stable, ion-locked conformation that represents the functional state present at the c-ring/membrane interface during rotation. This structure reveals a new, third type of ion coordination in ATP synthases. It appears in the ion binding site of an alkaliphile in which it represents a finely tuned adaptation of the proton affinity during the reaction cycle.
Source/Fonte: Uncommon Descent
Author Summary
Like the wind turbines that generate electricity, the F1Fo-ATP synthases are natural “ion turbines” each made up of a stator and a rotor that turns, when driven by a flow of ions, to generate the cell's energy supply of ATP. The Fo motor rotates by reversible binding and release of coupling ions that flow down the electrochemical ion gradient across the cytoplasmic cell membrane (in the case of bacteria) or intracellular organelle membranes (in the case of eukaryotic cells). Here, we present the structure of a rotor (c-)ring from a Bacillus species (B. pseudofirmus OF4) determined at high-resolution by X-ray crystallography. This bacterium prefers alkaline environments where the concentration of protons (H+) is lower outside than inside the cell – the inverse of the situation usually found in organisms that prefer neutral or acidic environments. The amino acid sequence of the protein subunits in this rotor, nevertheless, has features common to an important group of ATP synthases in organisms from bacteria to man. The structure reveals a new type of ion binding in which a protonated glutamate residue in the protein associates with a water molecule. This finding raises the possibility considered by Nobel laureate Paul Boyer several decades ago that a hydronium ion (a protonated water molecule, H3O+), rather than a proton alone, might be the coupling species that energizes ATP synthesis. Also, it demonstrates the finely tuned adaptation of ATP synthase rotor rings and their ion-binding sites to the specific requirements of different organisms.
Citation: Preiss L, Yildiz Ö, Hicks DB, Krulwich TA, Meier T (2010) A New Type of Proton Coordination in an F1Fo-ATP Synthase Rotor Ring. PLoS Biol 8(8): e1000443. doi:10.1371/journal.pbio.1000443
Academic Editor: John Kuriyan, University of California Berkeley, United States of America
Received: March 10, 2010; Accepted: June 24, 2010; Published: August 3, 2010
Copyright: © 2010 Preiss et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported in parts by the Cluster of Excellence “Macromolecular Complexes” at the Goethe University Frankfurt (DFG Project EXC 115), the DFG Collaborative Research Center 807 (to TM), and a research grant GM28454 from the National Institute of General Medical Sciences (to TAK). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: ATP, adenosine 5'-triphosphate; DCCD, N,N'-dicyclohexyl-carbodiimide; NCD-4, N-cyclohexyl-N'-(4-dimethylamino-α-naphthyl)carbodiimide ; pmf, proton motive force; smf, sodium motive force
* E-mail: thomas.meier@biophys.mpg.de
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