The c-ring stoichiometry of ATP synthase is adapted to cell physiological requirements of alkaliphilic Bacillus pseudofirmus OF4

Laura Preiss, Adriana L. Klyszejko, David B. Hicks, Jun Liu, Oliver J. Fackelmayer, Özkan Yildiz, Terry A. Krulwich, Thomas Meier

Research output: Contribution to journalArticlepeer-review

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Abstract

The c-rings of ATP synthases consist of individual c-subunits, all of which harbor a conserved motif of repetitive glycine residues (GxGxGxG) important for tight transmembrane α-helix packing. The cring stoichiometry determines the number of ions transferred during enzyme operation and has a direct impact on the ion-to-ATP ratio, a cornerstone parameter of cell bioenergetics. In the extreme alkaliphile Bacillus pseudofirmus OF4, the glycine motif is replaced by AxAxAxA. We performed a structural study on two mutants with alanine-to-glycine changes using atomic force microscopy and X-ray crystallography, and found that mutants form smaller c12 rings compared with the WT c13. The molar growth yields of B. pseudofirmus OF4 cells on malate further revealed that the c12 mutants have a considerably reduced capacity to grow on limitingmalate at high pH. Our results demonstrate that the mutant ATP synthases with either c12 or c13 can support ATP synthesis, and also underscore the critical importance of an alanine motif with c13 ring stoichiometry for optimal growth at pH >10. The data indicate a direct connection between the precisely adapted ATP synthase c-ring stoichiometry and its ionto- ATP ratio on cell physiology, and also demonstrate the bioenergetic challenges and evolutionary adaptation strategies of extremophiles.

Original languageEnglish
Pages (from-to)7874-7879
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume110
Issue number19
DOIs
StatePublished - 7 May 2013

Keywords

  • FF-ATP synthase rotor
  • Membrane protein complex

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