Hydrogenosomes in the diplomonad Spironucleus salmonicida

Nature Communications

Volumn 4, Issue , 2013, Pages

  Jerlström Hultqvist, Jon ^a   Einarsson, Elin ^a   Xu, Feifei ^a   Hjort, Karin ^a   Ek, Bo ^a   Steinhauf, Daniel ^a   Hultenby, Kjell ^b   Bergquist, Jonas ^a   Andersson, Jan O ^a   Svärd, Staffan G ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; HYDROGEN; IRON SULFUR PROTEIN;

ADAPTATION; EUKARYOTE; EVOLUTIONARY BIOLOGY; FUNGUS; HYDROGEN; MITOCHONDRION; SALMONID;

ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; DIPLOMONADIDA; GENUS; GIARDIA; HYDROGENOSOME; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ASSEMBLY; SALMON; SPIRONUCLEUS SALMONICIDA;

DIPLOMONADIDA; HYDROGEN; HYDROGENASE; MITOCHONDRIA; MODELS, BIOLOGICAL; ORGANELLES; PHYLOGENY; PROTEOMICS; PYRUVATES;

EID: 84893346165     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3493     Document Type: Article

References (45)

1. Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623-630 (2006).
2. Hjort, K., Goldberg, A. V., Tsaousis, A. D., Hirt, R. P. & Embley, T. M. Diversity and reductive evolution of mitochondria among microbial eukaryotes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 713-727 (2010).
3. Emelyanov, V. V. & Goldberg, A. V. Fermentation enzymes of Giardia intestinalis, pyruvate:ferredoxin oxidoreductase and hydrogenase, do not localize to its mitosomes. Microbiol. 157, 1602-1611 (2011).
4. Lloyd, D., Ralphs, J. R. & Harris, J. C. Giardia intestinalis, a eukaryote without hydrogenosomes, produces hydrogen. Microbiol. 148, 727-733 (2002).
5. Tovar, J. et al. Mitochondrial remnant organelles of Giardia function in ironsulphur protein maturation. Nature 426, 172-176 (2003).
6. Horner, D. S., Foster, P. G. & Embley, T. M. Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 17, 1695-1709 (2000).
7. Millet, C. O., Cable, J. & Lloyd, D. The diplomonad fish parasite Spironucleus vortens produces hydrogen. J. Eukaryot. Microbiol. 57, 400-404 (2010).
8. Jerlstrom-Hultqvist, J., Einarsson, E. & Svard, S. G. Stable transfection of the diplomonad parasite Spironucleus salmonicida. Eukaryot. Cell 11, 1353-1361 (2012).
9. Lill, R. & Kispal, G. Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem. Sci. 25, 352-356 (2000).
10. Lantsman, Y., Tan, K. S., Morada, M. & Yarlett, N. Biochemical characterization of a mitochondrial-like organelle from Blastocystis sp. subtype 7. Microbiol. 154, 2757-2766 (2008).
11. Dagley, M. J. et al. The protein import channel in the outer mitosomal membrane of Giardia intestinalis. Mol. Biol. Evol. 26, 1941-1947 (2009).
12. Dolezal, P. et al. Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc. Natl Acad. Sci. USA 102, 10924-10929 (2005).
13. Jedelsky, P. L. et al. The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS One 6, e17285 (2011).
14. Regoes, A. et al. Protein import, replication, and inheritance of a vestigial mitochondrion. J. Biol. Chem. 280, 30557-30563 (2005).
15. Mulder, D. W. et al. Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydA(DeltaEFG). Nature 465, 248-251 (2010).
16. Mulder, D. W. et al. Insights into [FeFe]-hydrogenase structure, mechanism, and maturation. Structure 19, 1038-1052 (2011).
17. Schneider, R. E. et al. The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int. J. Parasitol. 41, 1421-1434 (2011).
18. Mukherjee, M., Brown, M. T., McArthur, A. G. & Johnson, P. J. Proteins of the glycine decarboxylase complex in the hydrogenosome of Trichomonas vaginalis. Eukaryot. Cell 5, 2062-2071 (2006).
19. Mukherjee, M., Sievers, S. A., Brown, M. T. & Johnson, P. J. Identification and biochemical characterization of serine hydroxymethyl transferase in the hydrogenosome of Trichomonas vaginalis. Eukaryot. Cell 5, 2072-2078 (2006).
20. Perkins, D. N., Pappin, D. J. C., Creasy, D. M. & Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (1999).
21. Andersson, J. O., Sjögren, Å. M., Davis, L. A. M., Embley, T. M. & Roger, A. J. Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr. Biol. 13, 94-104 (2003).
22. Millet, C. O., Lloyd, D., Coogan, M. P., Rumsey, J. & Cable, J. Carbohydrate and amino acid metabolism of Spironucleus vortens. Exp. Parasitol. 129, 17-26 (2011).
23. Putz, S. et al. Fe-Hydrogenase maturases in the hydrogenosomes of Trichomonas vaginalis. Eukaryot. Cell 5, 579-586 (2006).
24. Simpson, A. G. B. & Patterson, D. J. The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the 'excavata hypothesis'. Eur. J. Protistol. 35, 353-370 (1999).
25. Takishita, K. et al. Multigene phylogenies of diverse Carpediemonas-like organisms identify the closest relatives of 'amitochondriate' diplomonads and retortamonads. Protist. 163, 344-355 (2012).
26. Roxström-Lindquist, K. et al. Large genomic differences between the morphologically indistinguishable diplomonads Spironucleus barkhanus and Spironucleus salmonicida. BMC Genomics 11, 258 (2010).
27. Ringqvist, E. et al. Release of metabolic enzymes by Giardia in response to interaction with intestinal epithelial cells. Mol. Biochem. Parasitol. 159, 85-91 (2008).
28. Jerlstrom-Hultqvist, J., Stadelmann, B., Birkestedt, S., Hellman, U. & Svard, S. G. Plasmid vectors for proteomic analyses in Giardia: purification of virulence factors and analysis of the proteasome. Eukaryot. Cell 11, 864-873 (2012).
29. Reynolds, E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212 (1963).
30. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
31. Dolezal, P. et al. Frataxin, a conserved mitochondrial protein, in the hydrogenosome of Trichomonas vaginalis. Eukaryot. Cell 6, 1431-1438 (2007).
32. Carlton, J. M. et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315, 207-212 (2007).
33. Aurrecoechea, C. et al. GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Res. 37, D526-D530 (2009).
34. Spironucleus vortens assembly and EST sequences http://genome.jgi-psf. org/Spivo0/Spivo0.download.ftp.html (2012).
35. Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
36. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22, 2688-2690 (2006).
37. Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542 (2012).
38. Allalou, A. & Wahlby, C. BlobFinder, a tool for fluorescence microscopy image cytometry. Comput. Methods Programs Biomed. 94, 58-65 (2009).
39. Wisniewski, J. R., Zougman, A., Nagaraj, N. & Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362 (2009).
40. Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896-1906 (2007).
41. Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786 (2011).
42. Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580 (2001).
43. Finn, R. D. et al. The Pfam protein families database. Nucleic Acids Res. 38, D211-D222 (2010).
44. HMMER 3.0 http://hmmer.org/ (2013).
45. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A. C. & Kanehisa, M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35, W182-W185 (2007).