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Were class C iron-containing superoxide dismutases of trypanosomatid parasites initially imported into a complex plastid? A hypothesis based on analyses of their N-terminal targeting signals

Published online by Cambridge University Press:  14 July 2008

A. BODYŁ  and
P. MACKIEWICZ
A. BODYŁ*
Affiliation:
Department of Biodiversity and Evolutionary Taxonomy, Zoological Institute, University of Wrocław, ul. Przybyszewskiego 63/77, 51-148 Wrocław, Poland
P. MACKIEWICZ
Affiliation:
Department of Genomics, Faculty of Biotechnology, University of Wrocław, ul. Przybyszewskiego 63/77, 51-148 Wrocław, Poland
*
*Corresponding author: Department of Biodiversity and Evolutionary Taxonomy, Zoological Institute, University of Wrocław, ul. Przybyszewskiego 63/77, 51-148 Wrocław, Poland. Fax: +48 71 322 28 17. E-mail: [email protected]
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Summary

Trypanosomatid parasites possess 2 distinct iron-containing superoxide dismutases (Fe-SODs) designated SODA and SODC, both of which are targeted to their mitochondria. In contrast to SODAs that carry typical mitochondrial transit peptides, SODCs have highly unusual mitochondrial targeting signals. Our analyses clearly show that these pre-sequences are bipartite possessing a signal peptide-like domain followed by a transit peptide-like domain. Consequently, they resemble N-terminal extensions of proteins targeted to multi-membrane plastids, suggesting that trypanosomatids once contained a eukaryotic alga-derived plastid. Further support for this hypothesis comes from striking similarities in length, hydropathy profile, and amino acid composition of SODC pre-sequences to those of Euglena and dinoflagellate plastid proteins. To account for these data, we propose that the Trypanosomatidae initially possessed a gene encoding a mitochondrial Fe-SOD with a classical mitochondrial transit peptide. Before or after plastid acquisition, a gene duplication event gave rise to SODA and SODC. In a subsequent evolutionary step a signal peptide was linked to SODC, enabling its import into the plastid. When the trypanosomatid plastid subsequently was lost, natural selection favoured adaptation of the SODC N-terminal signal as a mitochondrial transit peptide and re-targeting to the mitochondrion.

Keywords

dinoflagellatesendosymbiosisEuglenaLeishmaniaplastidprotein targetingreactive oxygen speciessuperoxide dismutaseTrypanosoma
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 9 , August 2008 , pp. 1101 - 1110
Copyright
Copyright © 2008 Cambridge University Press

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References

REFERENCES

Abascal, F., Zardoya, R. and Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.CrossRefGoogle ScholarPubMed
Archibald, J. M., Longet, D., Pawlowski, J. and Keeling, P. J. (2003). A novel polyubiquitin structure in Cercozoa and Foraminifera: evidence for a new eukaryotic supergroup. Molecular Biology and Evolution 20, 62–66.CrossRefGoogle ScholarPubMed
Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 57, 289–300.Google Scholar
Bodył, A. (2005). Do plastid-related characters support the chromalveolate hypothesis? Journal of Phycology 41, 712–719.CrossRefGoogle Scholar
Bruce, B. D. (2001). The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochimica et Biophysica Acta 1541, 2–21.CrossRefGoogle ScholarPubMed
Brydges, S. D. and Carruthers, V. B. (2003). Mutation of an unusual mitochondrial targeting sequence of SODB2 produces multiple targeting fates in Toxoplasma gondii. Journal of Cell Science 116, 4675–4685.CrossRefGoogle ScholarPubMed
Dufernez, F., Yernaux, C., Gerbod, D., Noel, C., Chauvenet, M., Wintjens, R., Edgcomb, V. P., Capron, M., Opperdoes, F. R. and Viscogliosi, E. (2006). The presence of four iron-containing superoxide dismutase isozymes in trypanosomatidae: characterization, subcellular localization, and phylogenetic origin in Trypanosoma brucei. Free Radical Biology & Medicine 40, 210–225.CrossRefGoogle ScholarPubMed
Durnford, D. G. and Gray, M. W. (2006). Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryotic Cell 5, 2079–2091.CrossRefGoogle ScholarPubMed
Fink, R. C. and Scandalios, J. G. (2002). Molecular evolution and structure-function relationships of the superoxide dismutase gene families in angiosperms and their relationships to other eukaryotic and prokaryotic superoxide dismutases. Archives of Biochemistry and Biophysics 399, 19–36.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Gupta, S. K., Kececioglu, J. and Schaffer, A. A. (1995). Improving the practical space and time efficiency of the shortest-paths approach to sum-of-pairs multiple sequence alignment. Journal of Computational Biology 2, 459–472.CrossRefGoogle ScholarPubMed
Hannaert, V., Saavedra, E., Duffieux, F., Szikora, J. P., Rigden, D. J., Michels, P. A. and Opperdoes, F. R. (2003). Plant-like traits associated with metabolism of Trypanosoma parasites. Proceedings of the National Academy of Sciences, USA 100, 1067–1071.CrossRefGoogle ScholarPubMed
Hempel, F., Bozarth, A., Sommer, M. S., Zauner, S., Przyborski, J. M. and Maier, U. G. (2007). Transport of nuclear-encoded proteins into secondarily evolved plastids. Biological Chemistry 388, 899–906.CrossRefGoogle ScholarPubMed
Ishida, K. (2005). Protein targeting into plastids: a key to understanding the symbiogenetic acquisitions of plastids. Journal of Plant Research 118, 237–245.CrossRefGoogle ScholarPubMed
Kyte, J. and Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of protein. Journal of Molecular Biology 157, 105–132.CrossRefGoogle Scholar
Martin, W. and Borst, P. (2003). Secondary loss of chloroplasts in trypanosomes. Proceedings of the National Academy of Sciences, USA 100, 765–767.CrossRefGoogle ScholarPubMed
Neupert, W. and Herrmann, J. M. (2007). Translocation of proteins into mitochondria. Annual Review of Biochemistry 76, 723–749.CrossRefGoogle ScholarPubMed
Nicholas, K. B. and Nicholas, H. B. Jr. (1997). GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors.Google Scholar
Nozaki, H., Matsuzaki, M., Takahara, M., Misumi, O., Kuroiwa, H., Hasegawa, M., Shin-i, T., Kohara, Y., Ogasawara, N. and Kuroiwa, T. (2003). The phylogenetic position of red algae revealed by multiple nuclear genes from mitochondria-containing eukaryotes and an alternative hypothesis on the origin of plastids. Journal of Molecular Evolution 56, 485–497.CrossRefGoogle Scholar
Patron, N. J., Waller, R. F., Archibald, J. M. and Keeling, P. J. (2005). Complex protein targeting to dinoflagellate plastids. Journal of Molecular Biology 348, 1015–1024.CrossRefGoogle ScholarPubMed
Pino, P., Foth, B. J., Kwok, L. Y., Sheiner, L., Schepers, R., Soldati, T. and Soldati-Favre, D. (2007). Dual targeting of antioxidant and metabolic enzymes to the mitochondrion and the apicoplast of Toxoplasma gondii. PLoS Pathogens 3, e115.CrossRefGoogle Scholar
Priest, J. W. and Hajduk, S. L. (1996). In vitro import of the Rieske iron-sulfur protein by trypanosome mitochondria. Journal of Biological Chemistry 271, 20060–20069.CrossRefGoogle ScholarPubMed
Priest, J. W. and Hajduk, S. L. (2003). Trypanosoma brucei cytochrome c1 is imported into mitochondria along an unusual pathway. Journal of Biological Chemistry 278, 15084–15094.CrossRefGoogle ScholarPubMed
R Development Core Team. (2006). R: a Language Environment for Statistical Computing. Technical report. R Foundation for Statistical Computing, Vienna, Austria [available online at: http://www.r-projekt.org].Google Scholar
Scandalios, J. G. (2005). Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defences. Brazilian Journal of Medical and Biological Research 38, 995–1014.CrossRefGoogle Scholar
Simpson, A. G., Stevens, J. R. and Lukeš, J. (2006) The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology 22, 168–174.CrossRefGoogle ScholarPubMed
StatSoft, Inc. (2006). STATISTICA (Data Analysis Software System), Version 7.1. [available online at: http://www.statsoft.com].Google Scholar
Wilkinson, S. R., Prathalingam, S. R., Taylor, M. C., Ahmed, A., Horn, D. and Kelly, J. M. (2006). Functional characterisation of the iron superoxide dismutase gene repertoire in Trypanosoma brucei. Free Radical Biology & Medicine 40, 198–209.CrossRefGoogle ScholarPubMed
Wolfe-Simon, F., Grzebyk, D., Schofield, O. and Falkowski, P. G. (2005). The role and evolution of superoxide dismutases in algae. Journal of Phycology 41, 453–465.CrossRefGoogle Scholar
Yang, Z. (1997). PAML: a program package for phylogenetic analysis by maximum likelihood. Computer Applications in the BioSciences 13, 555–556.Google ScholarPubMed
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