The Expression of a Plant-type Ferredoxin Redox System provides Molecular Evidence for a Plastid in the Early Dinoflagellate Perkinsus marinus

Protist

Volumn 158, Issue 1, 2007, Pages 119-130

  Stelter, Kathrin ^a   El Sayed, Najib M ^b   Seeber, Frank ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b J CRAIG VENTER INSTITUTE   (United States)

Author keywords

Apicomplexa; ferredoxin; Perkinsozoa; plastid; transit peptide

Indexed keywords

APICOMPLEXA; CYANOBACTERIA; DINOPHYCEAE; EUKARYOTA; MOLLUSCA; OSTREIDAE; PERKINSEA; PERKINSUS MARINUS; PROTOZOA;

EID: 33845717210     PISSN: 14344610     EISSN: 16180941     Source Type: Journal    
DOI: 10.1016/j.protis.2006.09.003     Document Type: Article

References (73)

1. Abrahamsen M.S., Templeton T.J., Enomoto S., Abrahante J.E., Zhu G., Lancto C.A., Deng M., Liu C., Widmer G., Tzipori S., Buck G.A., Xu P., Bankier A.T., Dear P.H., Konfortov B.A., Spriggs H.F., Iyer L., Anantharaman V., Aravind L., and Kapur V. Complete genome sequence of the apicomplexan Cryptosporidium parvum. Science 304 (2004) 441-445
2. Archibald J.M., Rogers M.B., Toop M., Ishida K., and Keeling P.J. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci USA 100 (2003) 7678-7683
3. Armbrust E.V., Berges J.A., Bowler C., Green B.R., Martinez D., Putnam N.H., Zhou S., Allen A.E., Apt K.E., Bechner M., Brzezinski M.A., Chaal B.K., Chiovitti A., Davis A.K., Demarest M.S., Detter J.C., Glavina T., Goodstein D., Hadi M.Z., Hellsten U., Hildebrand M., Jenkins B.D., Jurka J., Kapitonov V.V., Kröger N., Lau W.W., Lane T.W., Larimer F.W., Lippmeier J.C., Lucas S., Medina M., Montsant A., Obornik M., Parker M.S., Palenik B., Pazour G.J., Richardson P.M., Rynearson T.A., Saito M.A., Schwartz D.C., Thamatrakoln K., Valentin K., Vardi A., Wilkerson F.P., and Rokhsar D.S. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306 (2004) 79-86
4. Asamizu E., Nakajima M., Kitade Y., Saga N., Nakamura Y., and Tabata S. Comparison of RNA expression profiles between the two generations of Porphyra yezoensis (Rhodophyta), based on expressed sequence tag frequency analysis. J Phycol 39 (2003) 923-930
5. Bachvaroff T.R., Sanchez-Puerta M.V., and Delwiche C.F. Rate variation as a function of gene origin in plastid-derived genes of peridinin-containing dinoflagellates. J Mol Evol 62 (2006) 42-52
6. Bertini I., Luchinat C., Provenzani A., Rosato A., and Vasos P.R. Browsing gene banks for Fe2S2 ferredoxins and structural modeling of 88 plant-type sequences: An analysis of fold and function. Proteins 46 (2002) 110-127
7. Bodyl A. Do plastid-related characters support the chromalveolate hypothesis?. J Phycol 41 (2005) 712-719
8. Borza T., Popescu C.E., and Lee R.W. Multiple metabolic roles for the nonphotosynthetic plastid of the green alga Prototheca wickerhamii. Eukaryot Cell 4 (2005) 253-261
9. Brown G.D., Hudson K.L., and Reece K.S. Multiple polymorphic sites at the ITS and ATAN loci in cultured isolates of Perkinsus marinus. J Eukaryot Microbiol 51 (2004) 312-320
10. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17 (2000) 540-552
11. Cavalier-Smith T. Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Phil Trans R Soc Lond B Biol Sci 358 (2003) 109-133
12. Ceccarelli E.A., Arakaki A.K., Cortez N., and Carrillo N. Functional plasticity and catalytic efficiency in plant and bacterial ferredoxin-NADP(H) reductases. Biochim Biophys Acta 1698 (2004) 155-165
13. Eisenreich W., Bacher A., Arigoni D., and Rohdich F. Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci 61 (2004) 1401-1426
14. Gornicki P. Apicoplast fatty acid biosynthesis as a target for medical intervention in apicomplexan parasites. Int J Parasitol 33 (2003) 885-896
15. Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 (2003) 696-704
16. Hackett J.D., Scheetz T.E., Yoon H.S., Soares M.B., Bonaldo M.F., Casavant T.L., and Bhattacharya D. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics 6 (2005) 80
17. Hackett JD., Yoon H.S., Soares M.B., Bonaldo M.F., Casavant T.L., Scheetz T.E., Nosenko T., and Bhattacharya D. Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr Biol 14 (2004) 213-218
18. Hagopian J.C., Reis M., Kitajima J.P., Bhattacharya D., and de Oliveira M.C. Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodoplasts and their relationship to other plastids. J Mol Evol 59 (2004) 464-477
19. Hanke G.T., Okutani S., Satomi Y., Takao T., Suzuki A., and Hase T. Multiple iso-proteins of FNR in Arabidopsis: evidence for different contributions to chloroplast function and nitrogen assimilation. Plant Cell Environ 28 (2005) 1146-1157
20. Harb O.S., Chatterjee B., Fraunholz M.J., Crawford M.J., Nishi M., and Roos D.S. Multiple functionally redundant signals mediate targeting to the apicoplast in the apicomplexan parasite Toxoplasma gondii. Eukaryot Cell 3 (2004) 663-674
21. Jelenska J., Crawford M.J., Harb O.S., Zuther E., Haselkorn R., Roos D.S., and Gornicki P. Subcellular localization of acetyl-CoA carboxylase in the apicomplexan parasite Toxoplasma gondii. Proc Natl Acad Sci USA 98 (2001) 2723-2728
22. Jenni S., Leibundgut M., Maier T., and Ban N. Architecture of a fungal fatty acid synthase at 5 A° resolution. Science 311 (2006) 1263-1267
23. Jomaa H., Wiesner J., Sanderbrand S., Altincicek B., Weidemeyer C., Hintz M., Turbachova I., Eberl M., Zeidler J., Lichtenthaler H.K., Soldati D., and Beck E. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 285 (1999) 1573-1576
24. Keeling P.J., Burger G., Durnford D.G., Lang B.F., Lee R.W., Pearlman R.E., Roger A.J., and Gray M.W. The tree of eukaryotes. Trends Ecol Evol 20 (2005) 670-676
25. Leander BS., and Keeling P.J. Morphostasis in alveolate evolution. Trends Ecol Evol 18 (2003) 395-402
26. Leander B.S., and Keeling P.J. Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from hsp90 and actin phylogenies. J Phycol 40 (2004) 341-350
27. Li S., Nosenko T., Hackett J.D., and Bhattacharya D. Phylogenomic analysis identifies red algal genes of endosymbiotic origin in the chromalveolates. Mol Biol Evol 23 (2006) 663-674
28. Lidie K.B., Ryan J.C., Barbier M., and Van Dolah F.M. Gene expression in Florida red tide dinoflagellate Karenia brevis: analysis of an expressed sequence tag library and development of DNA microarray. Mar Biotechnol 7 (2005) 481-493
29. Liu B., Wang Y., Fillgrove K.L., and Anderson V.E. Triclosan inhibits enoyl-reductase of type I fatty acid synthase in vitro and is cytotoxic to MCF-7 and SKBr-3 breast cancer cells. Cancer Chemother Pharmacol 49 (2002) 187-193
30. Lund E.D., Soudant P., Chu F.L., Harvey E., Bolton S., and Flowers A. Effects of triclosan on growth, viability and fatty acid synthesis of the oyster protozoan parasite Perkinsus marinus. Dis Aquat Organ 67 (2005) 217-224
31. Lygre H., Moe G., Skalevik R., and Holmsen H. Interaction of triclosan with eukaryotic membrane lipids. Eur J Oral Sci 111 (2003) 216-222
32. McFadden G.I., Waller R.F., Reith M.E., and Lang-Unnasch N. Plastids in apicomplexan parasites. Plant Syst Evol (Suppl) 11 (1997) 261-287
33. McLeod R., Muench S.P., Rafferty J.B., Kyle D.E., Mui E.J., Kirisits M.J., Mack D.G., Roberts C.W., Samuel B.U., Lyons R.E., Dorris M., Milhous W.K., and Rice D.W. Triclosan inhibits the growth of Plasmodium falciparum and Toxoplasma gondii by inhibition of apicomplexan Fab I. Int J Parasitol 31 (2001) 109-113
34. Medina-Acosta E., and Cross G.A. Rapid isolation of DNA from trypanosomatid protozoa using a simple 'mini-prep' procedure. Mol Biochem Parasitol 59 (1993) 327-329
35. Mohamed M.E., Zaar A., Ebenau-Jehle C., and Fuchs G. Reinvestigation of a new type of aerobic benzoate metabolism in the proteobacterium Azoarcus evansii. J Bacteriol 183 (2001) 1899-1908
36. Newton A.P., Cadena S.M., Rocha M.E., Carnieri E.G., and Martinelli de Oliveira M.B. Effect of triclosan (TRN) on energy-linked functions of rat liver mitochondria. Toxicol Lett 160 (2005) 49-59
37. Noren F., Moestrup Ø., and Rehnstam-Holm A.S. Parvilucifera infectans Noren et Moestrup gen. et sp nov (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Europ J Protistol 35 (1999) 233-254
38. Ohta N., Matsuzaki M., Misumi O., Miyagishima S.Y., Nozaki H., Tanaka K., Shin I.T., Kohara Y., and Kuroiwa T. Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10 (2003) 67-77
39. Okada K., and Hase T. Cyanobacterial non-mevalonate pathway: (E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase interacts with ferredoxin in Thermosynechococcus elongatus BP-1. J Biol Chem 280 (2005) 20672-20679
40. Okamoto O.K., and Hastings J.W. Novel dinoflagellate clock-related genes identified through microarray analysis. J Phycol 39 (2003) 519-526
41. Okutani S., Hanke G.T., Satomi Y., Takao T., Kurisu G., Suzuki A., and Hase T. Three maize leaf ferredoxin:NADPH oxidoreductases vary in subchloroplast location, expression, and interaction with ferredoxin. Plant Physiol 139 (2005) 1451-1459
42. Pandini V., Caprini G., Thomsen N., Aliverti A., Seeber F., and Zanetti G. Ferredoxin-NADP+ reductase and ferredoxin of the protozoan parasite Toxoplasma gondii interact productively in vitro and in vivo. J Biol Chem 277 (2002) 48463-48471
43. Patron N.J., Waller R.F., Archibald J.M., and Keeling P.J. Complex protein targeting to dinoflagellate plastids. J Mol Biol 348 (2005) 1015-1024
44. Patron N.J., Waller R.F., and Keeling P.J. A tertiary plastid uses genes from two endosymbionts. J Mol Biol 357 (2006) 1373-1382
45. Paul K.S., Bacchi C.J., and Englund P.T. Multiple triclosan targets in Trypanosoma brucei. Eukaryot Cell 3 (2004) 855-861
46. Perkins F.O. The structure of Perkinsus marinus (Mackin, Owen and Collier, 1950) Levine, 1978 with comments on taxonomy and phylogeny of Perkinsus spp. J Shellfish Res 15 (1996) 67-87
47. Poirot O., Suhre K., Abergel C., O'Toole E., and Notredame C. 3DCoffee@igs: a web server for combining sequences and structures into a multiple sequence alignment. Nucleic Acids Res 32 (2004) W37-W40
48. Robledo J.A., Courville P., Cellier M.F., and Vasta G.R. Gene organization and expression of the divalent cation transporter Nramp in the protistan parasite Perkinsus marinus. J Parasitol 90 (2004) 1004-1014
49. Röhrich R.C., Englert N., Troschke K., Reichenberg A., Hintz M., Seeber F., Balconi E., Aliverti A., Zanetti G., Köhler U., Pfeiffer M., Beck E., Jomaa H., and Wiesner J. Reconstitution of an apicoplast-localised electron transfer pathway involved in the isoprenoid biosyntheis of Plasmodium falciparum. FEBS Lett 579 (2005) 6433-6438
50. Saldarriaga J.F., McEwan M.L., Fast N.M., Taylor F.J., and Keeling P.J. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. Int J Syst Evol Microbiol 53 (2003) 355-365
51. Saldarriaga J.F., Taylor F.J.R., Cavalier-Smith T., Menden-Deuer S., and Keeling P.J. Molecular data and the evolutionary history of dinoflagellates. Europ J Protistol 40 (2004) 85-111
52. Schott E.J., Robledo J.A., Wright A.C., Silva A.M., and Vasta G.R. Gene organization and homology modeling of two iron superoxide dismutases of the early branching protist Perkinsus marinus. Gene 309 (2003) 1-9
53. Seeber F., Aliverti A., and Zanetti G. The plant-type ferredoxin-NADP+ reductase/ferredoxin redox system as a possible drug target against apicomplexan human parasites. Curr Pharm Des 11 (2005) 3159-3172
54. Seemann M., Tse Sum Bui B., Wolff M., Miginiac-Maslow M., and Rohmer M. Isoprenoid biosynthesis in plant chloroplasts via the MEP pathway: direct thylakoid/ferredoxin-dependent photoreduction of GcpE/IspG. FEBS Lett 580 (2006) 1547-1552
55. Siddall M.E., Reece K.S., Graves J.E., and Burreson E.M. 'Total evidence' refutes the inclusion of Perkinsus species in the phylum Apicomplexa. Parasitology 115 (1997) 165-176
56. Sunila I., Hamilton R.M., and Dungan C.F. Ultrastructural characteristics of the in vitro cell cycle of the protozoan pathogen of oysters, Perkinsus marinus. J Eukaryot Microbiol 48 (2001) 348-361
57. Surolia N., and Surolia A. Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat Med 7 (2001) 167-173
58. Tong L. Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery. Cell Mol Life Sci 62 (2005) 1784-1803
59. Villalain J., Mateo C.R., Aranda F.J., Shapiro S., and Micol V. Membranotropic effects of the antibacterial agent Triclosan. Arch Biochem Biophys 390 (2001) 128-136
60. Villalba A., Reece K.S., Ordas M.C., Casas S.M., and Figueras A. Perkinsosis in molluscs: a review. Aquat Living Resour 17 (2004) 411-432
61. Vollmer M., Thomsen N., Wiek S., and Seeber F. Apicomplexan parasites possess distinct nuclear encoded but apicoplast-localized plant-type ferredoxin-NADP+ -reductase and ferredoxin. J Biol Chem 276 (2001) 5483-5490
62. Waller R.F., Patron N.J., and Keeling P.J. Phylogenetic history of plastid-targeted proteins in the peridinin-containing dinoflagellate Heterocapsa triquetra. Int J Syst Evol Microbiol 56 (2006) 1439-1447
63. Waller R.F., Ralph S.A., Reed M.B., Su V., Douglas J.D., Minnikin D.E., Cowman A.F., Besra G.S., and McFadden G.I. A type II pathway for fatty acid biosynthesis presents drug targets in Plasmodium falciparum. Antimicrob Agents Chemother 47 (2003) 297-301
64. Wang L.Q., Falany C.N., and James M.O. Triclosan as a substrate and inhibitor of 3'-phosphoadenosine 5'-phosphosulfate-sulfotransferase and UDP-glucuronosyl transferase in human liver fractions. Drug Metab Dispos 32 (2004) 1162-1169
65. White S.W., Zheng J., Zhang Y.M., and Rock K. The structural biology of type II fatty acid biosynthesis. Annu Rev Biochem 74 (2005) 791-831
66. Wiesner J., and Seeber F. The plastid-derived organelle of protozoan human parasites as a target of established and emerging drugs. Expert Opin Ther Targets 9 (2005) 23-44
67. Wright A.C., Ahmed H., Gauthier J.D., Silva A.M., and Vasta G.R. cDNA cloning and characterization of two iron superoxide dismutases from the oyster parasite Perkinsus marinus. Mol Biochem Parasitol 123 (2002) 73-77
68. Xu P., Widmer G., Wang Y., Ozaki L.S., Alves J.M., Serrano M.G., Puiu D., Manque P., Akiyoshi D., Mackey A.J., Pearson W.R., Dear P.H., Bankier A.T., Peterson D.L., Abrahamsen M.S., Kapur V., Tzipori S., and Buck G.A. The genome of Cryptosporidium hominis. Nature 431 (2004) 1107-1112
69. Yarlett N. Anaerobic protists and hidden mitochondria. Microbiology 150 (2004) 1127-1129
70. Yoon H.S., Hackett J.D., Van Dolah F.M., Nosenko T., Lidie K.L., and Bhattacharya D. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol Biol Evol 22 (2005) 1299-1308
71. Zagnitko O., Jelenska J., Tevzadze G., Haselkorn R., and Gornicki P. An isoleucine/leucine residue in the carboxyltransferase domain of acetyl-CoA carboxylase is critical for interaction with aryloxyphenoxypropionate and cyclohexanedione inhibitors. Proc Natl Acad Sci USA 98 (2001) 6617-6622
72. Zanetti G., Binda C., and Aliverti A. The [2Fe-2S] Ferredoxins. In: Messerschmidt A., Huber R., Poulos T., and Wieghardt K. (Eds). Handbook of Metalloproteins, Vol. 1 (2001), Wiley, Chichester 532-542
73. Zuther E., Johnson J.J., Haselkorn R., McLeod R., and Gornicki P. Growth of Toxoplasma gondii is inhibited by aryloxyphenoxypropionate herbicides targeting acetyl-CoA carboxylase. Proc Natl Acad Sci USA 96 (1999) 13387-13392