Mitochondrial genome of a tertiary endosymbiont retains genes for electron transport proteins

Journal of Eukaryotic Microbiology

Volumn 54, Issue 2, 2007, Pages 146-153

  Imanian, Behzad ^a   Carpenter, Kevin J ^a   Keeling, Patrick J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Cytochrome b; Cytochrome c oxidase 1; Cytochrome oxidase 3; Endosymbiosis; Kryptoperidinium foliaceum; Reductive evolution; Type II introns; Ultrastructure

Indexed keywords

CYTOCHROME B; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; PROTOZOAL DNA; PROTOZOAL PROTEIN;

DINOFLAGELLATE; ENDOSYMBIONT; ENZYME; GENE EXPRESSION; MITOCHONDRIAL DNA; PLASTID; PROTEIN; ULTRASTRUCTURE;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; DINOFLAGELLATE; DNA SEQUENCE; ELECTRON TRANSPORT; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SYMBIOSIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; CYTOCHROMES B; DINOFLAGELLIDA; DNA, MITOCHONDRIAL; DNA, PROTOZOAN; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX IV; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

BACILLARIOPHYTA; DINOPHYCEAE; KRYPTOPERIDINIUM FOLIACEUM; TUBULOCRISTATA;

EID: 34047097354     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2007.00245.x     Document Type: Article

References (55)

1. Archibald, J. M. & Keeling, P. J. 2002. Recycled plastids: a 'green movement' in eukaryotic evolution. Trends. Genet., 18:577-584.
2. Bhattacharya, D., Yoon, H. S. & Hackett, J. D. 2004. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. Bioessays, 26:50-60.
3. Bruno, W. J., Socci, N. D. & Halpern, A. L. 2000. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol., 17:187-197.
4. Bui, E. T. N. & Johnson, P. J. 1996. Identification and characterization of (Fe)-hydrogenases in the hydrogenosome of Trichomonas vaginalis. Mol. Biochem. Parasitol., 76:305-310.
5. Carty, S. & Cox, E. R. 1986. Kansodinium new-genus and Durinskia new-genus two genera of freshwater dinoflagellates pyrrophyta. Phycologia, 25:197-204.
6. Chesnick, J. M. & Cox, E. R. 1989. Fertilization and zygote development in the binucleate dinoflagellate Peridinium balticum (Pyrrhophyta). Am. J. Bot., 76:1060-1072.
7. Chesnick, J. M., Morden, C. W. & Schmieg, A. M. 1996. Identity of the endosymbiont of Peridinium foliaceum (Pyrrophyta): analysis of the rbcLS operon. J. Phycol., 32:850-857.
8. Chesnick, J. M., Kooistra, W. H. C., Wellbrock, U. & Medlin, L. K. 1997. Ribosomal RNA analysis indicates a benthic pennate diatom ancestry for the endosymbionts of the dinoflagellates Peridinium foliaceum and Peridinium balticum (Pyrrophyta). J. Eukaryot. Microbiol., 44:314-320.
9. Dodge, J. D. 1971. A dinoflagellate with both a mesokaryotic and a eukaryotic nucleus. Part 1: fine structure of the nuclei. Protoplasma, 73:145-157.
10. Dodge, J. D. 1983. The functional and phylogenetic significance of dinoflagellate eyespots. Biosystems, 16:259-268.
11. Douglas, S. E., Zauner, S., Fraunholz, M., Beaton, M., Penny, S., Deng, L., Wu, X., Reith, M., Cavalier-Smith, T. & Maier, U.-G. 2001. The highly reduced genome of an enslaved algal nucleus. Nature, 410:1091- 1096.
12. Ehara, M., Watanabe, K. I. & Ohama, T. 2000. Distribution of cognates of group II introns detected in mitochondrial cox1 genes of a diatom and a haptophyte. Gene, 256:157-167.
13. Fast, N. M., Kissinger, J. C., Roos, D. S. & Keeling, P. J. 2001. Nuclear-encoded, plastid-targeted genes suggest a single common origin for Apicomplexan and dinoflagellate plastids. Mol. Biol. Evol., 18:418-426.
14. Fields, S. D. & Rhodes, R. G. 1991. Ingestion and retention of Chromonas spp. (Cryptophyceae) by Gymnodinium acidotum (Dinophyceae). J. Phycol., 27:525-529.
15. Fontaine, J. M., Goux, D., Kloareg, B. & Loiseaux-de Goe, S. 1997. The reverse-transcriptase-like proteins encoded by group II introns in the mitochondrial genome of the brown alga Pylaiella littoralis belong to two different lineages which apparently coevolved with the group II ribozyme lineages. J. Mol. Evol., 44:33-42.
16. Gilson, P. R. & McFadden, G. I. 2002. Jam packed genomes: a preliminary, comparative analysis of nucleomorphs. Genetica, 115:13-28.
17. Gilson, P. R., Su, V., Slamovits, C. H., Reith, M. E., Keeling, P. J. & McFadden, G. I. 2006. Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus.. Proc. Natl. Acad. Sci. USA, 103:9566-9571.
18. Gray, M. W., Burger, G. & Lang, B. F. 1999. Mitochondrial evolution. Science, 283:1476-1481.
19. Guindon, S. & Gascuel, O. 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst. Biol., 53:696-704.
20. Hackett, J. D., Maranda, L., Yoon, H. S. & Bhattacharya, D. 2003. Phylogenetic evidence for the cryptophyte origin of the plastid of Dinophysis (Dinophysiales, dinophyceae). J. Phycol., 39:440-448.
21. Harper, J. T., Waanders, E. & Keeling, P. J. 2005. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int. J. Syst. Evol. Microbiol., 55:487-496.
22. Hewes, C. D., Mitchell, B. G., Moisan, T. A., Vernet, M. & Reid, F. M. H. 1998. The phycobilin signatures of chloroplasts from three dinoflagellate species: a microanalytical study of Dinophysis caudata, D. fortii and D. acuminata (Dinophysiales, Dinophyceae). J. Phycol., 34:945-951.
23. Horiguchi, T. & Pienaar, R. N. 1991. Ultrastructure of a marine dinoflagellate, Peridinium quinquecorne Abe (Peridiniales) from South Africa with special reference to its chrysophyte endosymbiont. Botanica Marina, 34:123-131.
24. Horiguchi, T. & Pienaar, R. N. 1994. Ultrastructure of a new marine sand-dwelling dinoflagellate, Gymnodinium quadrilobatum sp. Nov. (Dinophyceae) with special reference to its endosymbiotic alga. Eur. J. Phycol., 29:237-245.
25. Inagaki, Y., Dacks, J. B., Doolittle, W. F., Watanabe, K. I. & Ohama, T. 2000. Evolutionary relationship between dinoflagellates bearing obligate diatom endosymbionts: insight into tertiary endosymbiosis. Int. J. Syst. Evol. Microbiol., 50:2075-2081.
26. Ishida, K.-I., Cao, Y., Okada, N. & Hara, Y. 1997. The origin of chlorarachniophyte plastids, as inferred from phylogenetic comparisons of amino acid sequences of EF-Tu. J. Mol. Evol., 45:682-687.
27. Jeffrey, S. W. & Vesk, M. 1976. Further evidence for a membrane bound endosymbiont within the dinoflagellate Peridinium foliaceum. J. Phycol., 12:450-455.
28. Keeling, P. J., Burger, G., Durnford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J. & Gray, M. W. 2005. The tree of eukaryotes. Trends. Ecol. Evol., 20:670-676.
29. Kite, G. C., Rothschild, L. J. & Dodge, J. D. 1988. Nuclear and plastid dnas from the binucleate dinoflagellates Glenodinium foliaceum and Peridinium balticum. Biosystems, 21:151-164.
30. Lambowitz, A. M. & Belfort, M. 1993. Introns as mobile genetic elements. Annu. Rev. Biochem., 62:587-622.
31. Lewitus, A. J., Glasgow, H. B. & Burkholder, J. M. 1999. Kleptoplastidy in the toxic dinoflagellate Pfiesteria piscicida (Dinophyceae). J. Phycol., 35:303-312.
32. Lin, S., Zhang, H., Spencer, D. F., Norman, J. E. & Gray, M. W. 2002. Widespread and extensive editing of mitochondrial mrnas in dinoflagellates. J. Mol. Biol., 320:727-739.
33. Lucas, I. A. N. 1991. Symbionts of the tropical Dinophysiales (Dinophyceae). Ophelia, 33:213-224.
34. McEwan, M. & Keeling, P. J. 2004. HSP90, tubulin and actin are retained in the tertiary endosymbiont genome of Kryptoperidinium foliaceum. J. Eukaryot. Microbiol., 51:651-659.
35. McFadden, G. I. 2001. Primary and secondary endosymbiosis and the origin of plastids. J. Phycol., 37:951-959.
36. Michel, F. & Ferat, J. L. 1995. Structure and activities of group II introns. Annu. Rev. Biochem., 64:435-461.
37. Michel, F., Umesono, K. & Ozeki, H. 1989. Comparative and functional anatomy of group II catalytic introns: a review. Gene, 82:5-30.
38. Okamoto, N. & Inouye, I. 2005. A secondary symbiosis in progress? Science, 310:287.
39. Palmer, J. D. 2003. The symbiotic birth and spread of plastids: how many times and whodunit? J. Phycol., 39:4-11.
40. Roger, A. J. 1999. Reconstructing early events in eukaryotic evolution. Am. Nat., 154:S146-S163.
41. Rumpho, M. E., Summer, E. J., Green, B. J., Fox, T. C. & Manhart, J. R. 2001. Mollusc/algal chloroplast symbiosis: how can isolated chloroplasts continue to function for months in the cytosol of a sea slug in the absence of an algal nucleus? Zoology, 104:303-312.
42. Schmidt, H. A., Strimmer, K., Vingron, M. & Haeseler, A. V. 2002. Tree-puzzle: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics, 18:502-504.
43. Schnepf, E. & Elbraechter, M. 1988. Cryptophycean-like double membrane-bound chloroplast in the dinoflagellate, Dinophysis ehrenb evolutionary, phylogenetic and toxicological implications. Botanica Acta, 101:196-203.
44. Schweikert, M. & Elbraechter, M. 1999. A new form of endosymbiosis in Podolampas bipes Stein (Dinophyceae). J. Eukaryot. Microbiol., 46:12.
45. Tachezy, J., Sanchez, L. B. & Müller, M. 2001. Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of iscS. Mol. Biol. Evol., 18:1919-1928.
46. Tamura, M., Shimada, S. & Horiguchi, T. 2005. Galeidinium rugatum gen. Et sp. Nov. (Dinophyceae), a new coccoid dinoflagellate with a diatom endosymbiont. J. Phycol., 41:658-671.
47. Tengs, T., Dahlberg, O. J., Shalchian-Tabrizi, K., Klaveness, D., Rudi, K., Delwiche, C. F. & Jakobsen, K. S. 2000. Phylogenetic analyses indicate that the 19′hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol. Biol. Evol., 17:718-729.
48. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res., 22:4673-4680.
49. Tippit, D. H. & Pickett-Heaps, J. D. 1976. Apparent amitosis in the binucleate dinoflagellate Peridinium balticum. J. Cell. Sci., 21:273-289.
50. Van de Peer, Y. & De Wachter, R. 1997. Evolutionary relationship among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rrna. J. Mol. Evol., 45:615-630.
51. Van der Giezen, M., Tovar, J. & Clark, C. G. 2005. Mitochondrion-derived organelles in protists and fungi. Int. Rev. Cytol., 244:175-225.
52. Williams, B. A. P. & Keeling, P. J. 2003. Cryptic organelles in parasitic protists and fungi. Adv. Parasitol., 54:9-68.
53. Williams, B. A. P., Hirt, R. P., Lucocq, J. M. & Embley, T. M. 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature, 418:865-869.
54. Zhang, H. & Lin, S. 2005. Mitochondrial cytochrome b mrna editing in dinoflagellates: possible ecological and evolutionary associations? J. Eukaryot. Microbiol., 52:538-545.
55. Zhang, Z., Green, B. R. & Cavalier-Smith, T. 2000. Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J. Mol. Evol., 51:26-40.