Highly divergent mitochondrial ATP synthase complexes in tetrahymena thermophila

Praveen Balabaskaran Nina, Natalya V. Dudkina, Lesley A. Kane, Jennifer E. van Eyk, Egbert J. Boekema, Michael W. Mather, Akhil B. Vaidya

Research output: Contribution to journalArticle

Abstract

The F-type ATP synthase complex is a rotary nano-motor driven by proton motive force to synthesize ATP. Its F1 sector catalyzes ATP synthesis, whereas the Fo sector conducts the protons and provides a stator for the rotary action of the complex. Components of both F1 and Fo sectors are highly conserved across prokaryotes and eukaryotes. Therefore, it was a surprise that genes encoding the a and b subunits as well as other components of the Fo sector were undetectable in the sequenced genomes of a variety of apicomplexan parasites. While the parasitic existence of these organisms could explain the apparent incomplete nature of ATP synthase in Apicomplexa, genes for these essential components were absent even in Tetrahymena thermophila, a free-living ciliate belonging to a sister clade of Apicomplexa, which demonstrates robust oxidative phosphorylation. This observation raises the possibility that the entire clade of Alveolata may have invented novel means to operate ATP synthase complexes. To assess this remarkable possibility, we have carried out an investigation of the ATP synthase from T. thermophila. Blue native polyacrylamide gel electrophoresis (BN-PAGE) revealed the ATP synthase to be present as a large complex. Structural study based on single particle electron microscopy analysis suggested the complex to be a dimer with several unique structures including an unusually large domain on the intermembrane side of the ATP synthase and novel domains flanking the c subunit rings. The two monomers were in a parallel configuration rather than the angled configuration previously observed in other organisms. Proteomic analyses of well-resolved ATP synthase complexes from 2-D BN/BN-PAGE identified orthologs of seven canonical ATP synthase subunits, and at least 13 novel proteins that constitute subunits apparently limited to the ciliate lineage. A mitochondrially encoded protein, Ymf66, with predicted eight transmembrane domains could be a substitute for the subunit a of the Fo sector. The absence of genes encoding orthologs of the novel subunits even in apicomplexans suggests that the Tetrahymena ATP synthase, despite core similarities, is a unique enzyme exhibiting dramatic differences compared to the conventional complexes found in metazoan, fungal, and plant mitochondria, as well as in prokaryotes. These findings have significant implications for the origins and evolution of a central player in bioenergetics.

Original languageEnglish (US)
JournalPLoS Biology
Volume8
Issue number7
DOIs
StatePublished - Jul 2010

Fingerprint

Mitochondrial Proton-Translocating ATPases
Tetrahymena thermophila
H-transporting ATP synthase
Adenosine Triphosphate
Apicomplexa
Native Polyacrylamide Gel Electrophoresis
prokaryotic cells
Gene encoding
Ciliophora
polyacrylamide gel electrophoresis
Electrophoresis
Stator
Alveolata
Protons
Tetrahymena
Genes
oxidative phosphorylation
Gene Components
organisms
protein subunits

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

Nina, P. B., Dudkina, N. V., Kane, L. A., van Eyk, J. E., Boekema, E. J., Mather, M. W., & Vaidya, A. B. (2010). Highly divergent mitochondrial ATP synthase complexes in tetrahymena thermophila. PLoS Biology, 8(7). https://doi.org/10.1371/journal.pbio.1000418.g005

Highly divergent mitochondrial ATP synthase complexes in tetrahymena thermophila. / Nina, Praveen Balabaskaran; Dudkina, Natalya V.; Kane, Lesley A.; van Eyk, Jennifer E.; Boekema, Egbert J.; Mather, Michael W.; Vaidya, Akhil B.

In: PLoS Biology, Vol. 8, No. 7, 07.2010.

Research output: Contribution to journalArticle

Nina, PB, Dudkina, NV, Kane, LA, van Eyk, JE, Boekema, EJ, Mather, MW & Vaidya, AB 2010, 'Highly divergent mitochondrial ATP synthase complexes in tetrahymena thermophila', PLoS Biology, vol. 8, no. 7. https://doi.org/10.1371/journal.pbio.1000418.g005
Nina, Praveen Balabaskaran ; Dudkina, Natalya V. ; Kane, Lesley A. ; van Eyk, Jennifer E. ; Boekema, Egbert J. ; Mather, Michael W. ; Vaidya, Akhil B. / Highly divergent mitochondrial ATP synthase complexes in tetrahymena thermophila. In: PLoS Biology. 2010 ; Vol. 8, No. 7.
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