Journal of Molecular Evolution

, Volume 63, Issue 4, pp 504–512 | Cite as

Proteasome-Related HslU and HslV Genes Typical of Eubacteria Are Widespread in Eukaryotes

Article

Abstract

Many eubacteria contain an ATP-dependent protease complex, which is built by multiple copies of the HslV and HslU proteins and is therefore called HslVU. HslU proteins are AAA + ATPases, while HslV proteins are proteases that show highly significant similarity to β subunits of proteasomes. Therefore, the HslVU complex has been envisaged as a precursor or ancestral type of proteasome. Here we show that species of most of the main eukaryotic lineages have HslU and HslV genes very similar to those found in proteobacteria. We have detected them in amoebozoa, plantae, chromoalveolata, rhizaria, and excavata species. Phylogenetic analyses suggest that these genes have been obtained by endosymbiosis from the proteobacterial ancestor that gave rise to eukaryotic mitochondria. The products encoded by these eukaryotic genes adopt, according to modeling based on the known crystal structures of prokaryotic HslU and HslV proteins, conformations that are compatible with their being fully active, suggesting that functional HslVU complexes may be present in many eukaryotic species.

Keywords

HslVU complex Proteasome Protein quality control Early evolution Endosymbiosis Comparative genomics 

Notes

Acknowledgments

Our group is supported by Grants GEN2001-4851-C06-02 and SAF2003-09506 (Ministerio de Educación y Ciencia, Spain) and Grant GV04B-141 (Generalitat Valenciana, Spain).

References

  1. Bochtler M, Ditzel L, Groll M, Huber RR (1997) Crystal structure of heat shock locus V (HslV) from Escherichia coli. Proc Natl Acad Sci USA 94:6070–6074PubMedCrossRefGoogle Scholar
  2. Bochtler M, Hartmann C, Song HK, Bourenkov GP, Bartunik HD, Huber R (2000) The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 403:800–805PubMedCrossRefGoogle Scholar
  3. Bouzat JL, McNeil LK, Robertson HM, Solter LF, Nixon JE, Beever JE, Gaskins HR, Olsen G, Subramaniam S, Sogin ML, Lewin HA (2000) Phylogenomic analysis of the alpha proteasome gene family from early-diverging eukaryotes. J Mol Evol 51:532–543PubMedGoogle Scholar
  4. Cavalier-Smith T (2004) Only six kingdoms of life. Proc Biol Sci 271:1251–1262PubMedCrossRefGoogle Scholar
  5. Chuang SE, Burland V, Plunkett 3rd G, Daniels DL, Blattner FR (1993) Sequence analysis of four new heat-shock genes constituting the hslTS/ibpAB and hslVU operons in Escherichia coli. Gene 134:1–6PubMedCrossRefGoogle Scholar
  6. Couvreur B, Wattiez R, Bollen A, Falmagne P, Le Ray D, Dujardin JC (2002) Eubacterial HslV and HslU subunits homologs in primordial eukaryotes. Mol Biol Evol 19:2110–2117PubMedGoogle Scholar
  7. De Mot R, Nagy I, Walz J, Baumeister W (1999) Proteasomes and other self-compartmentalizing proteases in prokaryotes. Trends Microbiol 7:88–92PubMedCrossRefGoogle Scholar
  8. Gille C, Goede A, Schloetelburg C, Preissner R, Kloetzel PM, Gobel UB, Frommel C (2003) A comprehensive view on proteasomal sequences: implications for the evolution of the proteasome. J Mol Biol 326:1437–1448PubMedCrossRefGoogle Scholar
  9. Groll M, Bochtler M, Brandstetter H, Clausen T, Huber R (2005) Molecular machines for protein degradation. Chem Biochem 6:222–256Google Scholar
  10. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723PubMedCrossRefGoogle Scholar
  11. Hughes AL (1997) Evolution of the proteasome components. Immunogenetics 46:82–92PubMedCrossRefGoogle Scholar
  12. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  13. Lupas A, Zuhl F, Tamura T, Wolf S, Nagy I, De Mot R, Baumeister W (1997) Eubacterial proteasomes. Mol Biol Rep 24:125–131PubMedCrossRefGoogle Scholar
  14. Nicholas KB, Nicholas HB Jr (1997) GeneDoc: Analysis and visualization of genetic variation. Distributed by the authors; http://www.psc.edu/biomed/genedoc/
  15. Page RD (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  16. Peitsch MC (1996) ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. Biochem Soc Trans 24:274–279PubMedGoogle Scholar
  17. Richards TA, Cavalier-Smith T (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436:1113–1118PubMedCrossRefGoogle Scholar
  18. Rohrwild M, Pfeifer G, Santarius U, Muller SA, Huang HC, Engel A, Baumeister W, Goldberg AL (1997) The ATP-dependent HslVU protease from Escherichia coli is a four-ring structure resembling the proteasome. Nat Struct Biol 4:133–139PubMedCrossRefGoogle Scholar
  19. Simpson AG, Roger AJ (2004) The real ‘kingdoms’ of eukaryotes. Curr Biol 14:R693–R696PubMedCrossRefGoogle Scholar
  20. Sitnikova T, Rzhetsky A, Nei M (1995) Interior-branch and bootstrap tests of phylogenetic trees. Mol Biol Evol 12:319–333PubMedGoogle Scholar
  21. Song HK, Hartmann C, Ramachandran R, Bochtler M, Behrendt R, Moroder L, Huber R (2000) Mutational studies on HslU and its docking mode with HslV. Proc Natl Acad Sci USA 97:14103–14108PubMedCrossRefGoogle Scholar
  22. Sousa MC, Trame CB, Tsuruta H, Wilbanks SM, Reddy VS, McKay DB (2000) Crystal and solution structures of an HslUV protease-chaperone complex. Cell 103:633–643PubMedCrossRefGoogle Scholar
  23. Stechmann A, Cavalier-Smith T (2003) The root of the eukaryote tree pinpointed. Curr Biol 13:R665–R666PubMedCrossRefGoogle Scholar
  24. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  25. Volker C, Lupas AN (2002) Molecular evolution of proteasomes. Curr Top Microbiol Immunol 268:1–22PubMedGoogle Scholar
  26. Wang J, Song JJ, Franklin MC, Kamtekar S, Im YJ, Rho SH, Seong IS, Lee CS, Chung CH, Eom SH (2001) Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism. Structure 9:177–184PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Departamento de GenéticaUniversidad de ValenciaValenciaSpain
  2. 2.Department of ZoologySchool of Natural Sciences, University of Dublin Trinity CollegeIreland

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