A specific adaptation in the a subunit of thermoalkaliphilic F1FO-ATP synthase enables ATP synthesis at high pH but not at neutral pH values

J Biol Chem. 2007 Jun 15;282(24):17395-404. doi: 10.1074/jbc.M611709200. Epub 2007 Apr 13.

Abstract

Analysis of the atp operon from the thermoalkaliphilic Bacillus sp. TA2.A1 and comparison with other atp operons from alkaliphilic bacteria reveals the presence of a conserved lysine residue at position 180 (Bacillus sp. TA2.A1 numbering) within the a subunit of these F(1)F(o)-ATP synthases. We hypothesize that the basic nature of this residue is ideally suited to capture protons from the bulk phase at high pH. To test this hypothesis, a heterologous expression system for the ATP synthase from Bacillus sp. TA2.A1 (TA2F(1)F(o)) was developed in Escherichia coli DK8 (Deltaatp). Amino acid substitutions were made in the a subunit of TA2F(1)F(o) at position 180. Lysine (aK180) was substituted for the basic residues histidine (aK180H) or arginine (aK180R), and the uncharged residue glycine (aK180G). ATP synthesis experiments were performed in ADP plus P(i)-loaded right-side-out membrane vesicles energized by ascorbate-phenazine methosulfate. When these enzyme complexes were examined for their ability to perform ATP synthesis over the pH range from 7.0 to 10.0, TA2F(1)F(o) and aK180R showed a similar pH profile having optimum ATP synthesis rates at pH 9.0-9.5 with no measurable ATP synthesis at pH 7.5. Conversely, aK180H and aK180G showed maximal ATP synthesis at pH values 8.0 and 7.5, respectively. ATP synthesis under these conditions for all enzyme forms was sensitive to DCCD. These data strongly imply that amino acid residue Lys(180) is a specific adaptation within the a subunit of TA2F(1)F(o) to facilitate proton capture at high pH. At pH values near the pK(a) of Lys(180), the trapped protons readily dissociate to reach the subunit c binding sites, but this dissociation is impeded at neutral pH values causing either a blocking of the proposed H(+) channel and/or mechanism of proton translocation, and hence ATP synthesis is inhibited.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / biosynthesis*
  • Amino Acid Sequence
  • Bacillus / enzymology*
  • Bacillus / genetics
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Cell Membrane / metabolism
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Hydrogen-Ion Concentration*
  • Indicators and Reagents / metabolism
  • Mitochondrial Proton-Translocating ATPases / chemistry
  • Mitochondrial Proton-Translocating ATPases / genetics
  • Mitochondrial Proton-Translocating ATPases / metabolism*
  • Molecular Sequence Data
  • Mutation
  • Onium Compounds / metabolism
  • Operon
  • Protein Subunits / chemistry
  • Protein Subunits / genetics
  • Protein Subunits / metabolism*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Trityl Compounds / metabolism

Substances

  • Bacterial Proteins
  • Indicators and Reagents
  • Onium Compounds
  • Protein Subunits
  • Recombinant Proteins
  • Trityl Compounds
  • triphenylmethylphosphonium
  • Adenosine Triphosphate
  • F1F0-ATP synthase
  • Mitochondrial Proton-Translocating ATPases