Advertisement

Photosynthesis Research

, Volume 33, Issue 2, pp 137–146 | Cite as

Evolution of proton pumping ATPases: Rooting the tree of life

  • Johann Peter Gogarten
  • Lincoln Taiz
Minireview

Abstract

Proton pumping ATPases are found in all groups of present day organisms. The F-ATPases of eubacteria, mitochondria and chloroplasts also function as ATP synthases, i.e., they catalyze the final step that transforms the energy available from reduction/oxidation reactions (e.g., in photosynthesis) into ATP, the usual energy currency of modern cells. The primary structure of these ATPases/ATP synthases was found to be much more conserved between different groups of bacteria than other parts of the photosynthetic machinery, e.g., reaction center proteins and redox carrier complexes.

These F-ATPases and the vacuolar type ATPase, which is found on many of the endomembranes of eukaryotic cells, were shown to be homologous to each other; i.e., these two groups of ATPases evolved from the same enzyme present in the common ancestor. (The term eubacteria is used here to denote the phylogenetic group containing all bacteria except the archaebacteria.) Sequences obtained for the plasmamembrane ATPase of various archaebacteria revealed that this ATPase is much more similar to the eukaryotic than to the eubacterial counterpart. The eukaryotic cell of higher organisms evolved from a symbiosis between eubacteria (that evolved into mitochondria and chloroplasts) and a host organism. Using the vacuolar type ATPase as a molecular marker for the cytoplasmic component of the eukaryotic cell reveals that this host organism was a close relative of the archaebacteria.

A unique feature of the evolution of the ATPases is the presence of a non-catalytic subunit that is paralogous to the catalytic subunit, i.e., the two types of subunits evolved from a common ancestral gene. Since the gene duplication that gave rise to these two types of subunits had already occurred in the last common ancestor of all living organisms, this non-catalytic subunit can be used to root the tree of life by means of an outgroup; that is, the location of the last common ancestor of the major domains of living organisms (archaebacteria, eubacteria and eukaryotes) can be located in the tree of life without assuming constant or equal rates of change in the different branches.

A correlation between structure and function of ATPases has been established for present day organisms. Implications resulting from this correlation for biochemical pathways, especially photosynthesis, that were operative in the last common ancestor and preceding life forms are discussed.

Key words

ATPase progenote origin of life archaebacteria membrane transport 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bennett AB and Spanswick RM (1984) H+-ATPase activity from storage tissue of Beta vulgaris; II. H+/ATP stoichiometry of an anion-sensitive H+-ATPase. Plant Physiol 74: 545–548Google Scholar
  2. Blair HC, Teichelbaum SL, Ghiselli R and Gluck S (1989) Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245: 855–857PubMedGoogle Scholar
  3. Bowman BJ, Allen R, Wechser MA and Bowman EJ (1988) Isolation of genes encoding the Neurospora vacuolar ATPase: Analysis of vma-2 encoding the 57 kDa polypeptide and comparison to vma-1. J Biol Chem 263: 14002–14007PubMedGoogle Scholar
  4. Bowman BJ, Dschida WJ, Harris T and Bowman EJ (1989) The vacuolar ATPase of Neurospora crassa contains an F1-like structure. J Biol Chem 264: 15606–15612PubMedGoogle Scholar
  5. Cross RL and Taiz L (1990) Gene duplication as a means for altering H+/ATP ratios during the evolution. FEBS Lett 259: 227–229CrossRefPubMedGoogle Scholar
  6. Denda K, Konishi J, Oshima T, Date T and Yoshida M (1988a) Molecular cloning of the b subunit of a possible non-F0F1 type ATP synthase from the acidothermophilic archaebacterium Sulfolobus acidocaldarius. J Biol Chem 263: 17251–17254PubMedGoogle Scholar
  7. Denda K, Konishi J, Oshima T, Date T and Yoshida M (1988b) The membran associated ATPase from Sulfolobus acidocatdarius is distantly related to F1-ATPase as adressed from the primary structure of its A-subunit. J Biol Chem 263: 6012–6015PubMedGoogle Scholar
  8. Denda K, Konishi J, Oshima T, Date T and Yoshida M (1989) A gene encoding the proteolipid subunit of Sulfolobus acidocaldarius ATPase complex. J Biol Chem 264: 7119–7121PubMedGoogle Scholar
  9. Felsenstein J (1981) Evolutionary trees from DNA sequences: A maximum likelihood approch. J Mol Evol 17: 368–376PubMedGoogle Scholar
  10. Forgac M (1989) Structure and function of vacuolar class of ATP driven proton pumps. Physiological Rev 69: 765–796Google Scholar
  11. Gluck S and Cadwell J (1987) Immunoaffinity purification of vacuolar H+ ATPase. J Biol Chem 262: 15780–15787PubMedGoogle Scholar
  12. Gogarten JP, Kibak H, Taiz L, Bowman EJ, Bowman BJ, Manolson MF, Poole RJ, Date T, Oshima T, Konishi J, Denda K and Yoshida M (1989a) The evolution of the vacuolar H+-ATPase: Implications for the origin of eukaryotes. Proc Natl Acad Sci USA 86: 6661–6665PubMedGoogle Scholar
  13. Gogarten JP, Rausch T, Bernasconi P, Kibak H and Taiz L (1989b) Molecular evolution of H+-ATPase. I. Methanococcus and Sulfolobus are monophyletic with respect to eukaryotes and eubacteria. Z Naturforsch 44c: 641–650Google Scholar
  14. Ihara K and Mukohata Y (1991) The ATP Synthase of Halobacterium salinarium (halobium) is an archaebacterial type as revealed from the amino acid sequences of its two major subunits. Arch Biochem Biophys 286: 111–116PubMedGoogle Scholar
  15. Inatomi K-I, Eya S, Maeda M and Futai M (1989) Amino acid sequence of the alpha and beta subunits of Methanosarcina barkeri ATPase deduced from cloned genes. Similarity to subunits of eukaryotic vacuolar and F0F1-ATPases. J Biol Chem 264: 10954–10959Google Scholar
  16. Iwabe N, Kuma K-I, Hasegawa M, Osawa S and Miyata T (1989) Evolutionary relationships of archaebacteria, eubacteria and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci USA 86: 9355–9359PubMedGoogle Scholar
  17. Lake JA (1988) Origin of the eukaryotic nucleus determined by rate invariant analysis of rRNA sequences. Nature 331: 184–186CrossRefPubMedGoogle Scholar
  18. Manolson MF, Ouellette BF, Filion M and Poole RJ (1988) cDNA sequence and homologies of the ‘57-kDa’ nucleotide-binding subunit of the vacuolar ATPase from Arabidopsis. J Biol Chem 263: 17987–17994PubMedGoogle Scholar
  19. Mitchell P (1966) Chemiosmotic Coupling in Oxidative and Photosynthetic Coupling. Glynn Research Ltd, Bodmin, UKGoogle Scholar
  20. Nelson H and Nelson N (1989) The progenitor of ATP synthases was closely related to the current vacuolar H+-ATPase. FEBS Lett 247: 147–153CrossRefPubMedGoogle Scholar
  21. Pedersen PL and Carafioli E (1987) Ion motive ATPases. Trends Biochem Sci 12: 146–150 and 186–189CrossRefGoogle Scholar
  22. Taiz SL and Taiz L (1991) Ultrastructural comparison of the vacuolar and mitochondrial H+-ATPases of Daucus carota. Bot Acta 104: 117–121Google Scholar
  23. Woese CR (1987) Bacterial evolution. Microbiol Rev 51: 221–271PubMedGoogle Scholar
  24. Woese CR and Fox GE (1977a) Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc Natl Acad Sci USA 74: 5088–5090PubMedGoogle Scholar
  25. Woese CR and Fox GE (1977b) The concept of cellular evolution. J Mol Evol 10: 1–6PubMedGoogle Scholar
  26. Zimniak L, Dittrich P, Gogarten JP, Kibak H and Taiz L (1988) The cDNA sequence of the 69 kDa subunit of the carrot vacuolar H+-ATPase: Homology to the beta-chain of F0F1-ATPases. J Biol Chem 263: 9102–9112PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1992

Authors and Affiliations

  • Johann Peter Gogarten
    • 1
  • Lincoln Taiz
    • 2
  1. 1.Department of Molecular and Cell BiologyUniversity of ConnecticutStorrsUSA
  2. 2.Biology DepartmentUniversity of CaliforniaSanta CruzUSA

Personalised recommendations