Transcriptome sequencing reveals single domain Type I-like polyketide synthases in the toxic dinoflagellate Gambierdiscus polynesiensis

Harmful Algae

Volumn 36, Issue , 2014, Pages 29-37

  Pawlowiez, R ^a   Morey, J S ^b   Darius, H T ^a   Chinain, M ^a   Van Dolah, F M ^b  

^a INSTITUT LOUIS MALARDÉ   (French Polynesia)

^b CENTER FOR COASTAL ENVIRONMENTAL HEALTH AND BIOMOLECULAR RESEARCH   (United States)

Author keywords

Dinoflagellate; Fatty acid; Gambierdiscus polynesiensis; Polyketide synthase; Toxin biosynthesis; Transcriptomic analysis

Indexed keywords

EID: 84901503442     PISSN: 15689883     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hal.2014.04.013     Document Type: Article

References (54)

1. Aligizaki K., Nikolaidis G. Morphological identification of two tropical dinoflagellates of the genera Gambierdiscus and Sinophysis in the Mediterranean sea. J. Biol. Res. Thessalon 2008, 9:72-82.
2. Bachvaroff T.R., Place A.R. From stop to start: tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellates Amphidinium carterae. PLoS ONE 2008, 3(8):e2929.
3. Bagnis R., Chanteau S., Chungue E., Hurtel J.M., Yasumoto T., Inoue A. Origins of ciguatera fish poisoning: a new dinoflagellate Gambierdiscus toxicus Adachi and Fukuya, definitively involved as a causal agent. Toxicon 1980, 18(2):199-208.
4. Bomber J.W. Ecology, Genetic Variability and Physiology of the Ciguatera-Causing Dinoflagellate Gambierdiscus toxicus Adachi and Fukuyo 1987, (Ph.D. Thesis), Florida Institute of Technology, Melbourne, Florida, 147 pp.
5. Bruslé J. Ciguatera fish poisoning - a review. Sanitary and Economic Aspects 1997, Les éditions INSERM, Paris, France, 147 pp.
6. Chan D.I., Vogel H.J. Current understanding of fatty acid biosynthesis and the acyl carrier protein. Biochem. J. 2010, 430:1-19.
7. Chinain M., Darius H.T., Ung A., Cruchet P., Wang Z., Ponton D., Laurent D., Pauillac S. Growth and toxin production in the ciguatera-causing dinoflagellate Gambierdiscus polynesiensis (Dinophyceae) in culture. Toxicon 2010, 56:739-750.
8. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., Robles M. Blast2GO: a universal tool for annotation and visualization in functional genomics research. Bioinformatics 2005, 21(18):3674-3676.
9. de Haro L., Pommier P., Valli M. Emergence of imported ciguatera in Europe: report of 18 cases at the poison control center of Marseille. J. Toxicol. Clin. Toxicol. 2003, 41(7):927-930.
10. de Swaaf M.E., de Rijk T.C., van der Meer P., Eggink G., Sijtsma L. Analysis of docosahexaenoic acid biosynthesis in Crypthecodinium cohnii by C-13 labelling and desaturase inhibitor experiments. J. Biotechnol. 2003, 103:21-29.
11. Eichholz K., Beszteri B., John U. Putative monofunctional Type I polyketide synthase units: a dinoflagellate-specific feature?. PLoS ONE 2012, 7:e48624.
12. Fleming L.E., Baden D.G., Bean J.A., Weisman R., Blythe D.G. Seafood toxin diseases: issues in epidemiology and community outreach. Harmful Algae 1998, 245-248. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Galicia. B. Reguera, J. Blanco, M.L. Fernandez, T. Wyatt (Eds.).
13. Fraga S., Rodriguez F., Caillaud A., Diogene J., Raho N., Zapata M. Gambierdiscus excentricus sp. nov (Dinophyceae), a benthic toxic dinoflagellate from the Canary Islands (NE Atlantic Ocean). Harmful Algae 2011, 11:10-22.
14. Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., Chen Z., Mauceli E., Hacohen N., Gnirke A., Rhind N., di Palma F., Birren B.W., Nusbaum C., Lindblad-Toh K., Friedman N., Regev A. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat. Biotechnol. 2011, 29(7):644-652.
15. Hackett J.D., Scheetz T.E., Yoon H.S., Soares M.B., Bonaldo M.F., Casavant T.L., Bhattacharya D. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics 2005, 6:80.
16. Hirama M., Oishi T., Uehara H., Inoue M., Maruyama M., Oguri H., Satake M. Total synthesis of ciguatoxin CTX3C. Science 2001, 294:1904-1907.
17. Holmes M.J., Lewis R.J., Poli M.A., Gillepsie N. Strain dependent production of ciguatoxin precursors (Gambiertoxins) by Gambierdiscus toxicus (Dinophyceae) in culture. Toxicon 1991, 29(6):761-775.
18. Hopwood D.A. Genetic contributions to understanding polyketide synthases. Chem. Rev. 1997, 97:2465-2497.
19. Inoue M., Miyazaki K., Ishihara Y., Tatami A., Ohnuma Y., Kawada Y., Komano K., Yamashita S., Lee N., Hirama M. Total synthesis of ciguatoxin and 51-hydroxyCTX3C. J. Am. Chem. Soc. 2006, 128(26):9352-9354.
20. Inoue M., Miyazaki K., Uehara H., Maruyama M., Hirama M. First- and second-generation total synthesis of ciguatoxin CTX3C. Proc. Natl. Acad. Sci. U. S. A 2004, 101:12013-12018.
21. Inoue M., Uehara H., Maruyama M., Hirama M. Practical total synthesis of ciguatoxin CTX3C by improved group strategy. Org. Lett. 2002, 4(25):4551-4554.
22. Jenke-Kodama H., Dittmann E. Evolution of metabolic diversity: insights from microbial polyketide synthases. Phytochemistry 2009, 70:1858-1866.
23. Kalaitzis J.A., Chau R., Kohli G.S., Murray S.A., Neilan B.A. Biosynthesis of toxic naturally occurring seafood contaminants. Toxicon 2010, 56:244-258.
24. Kellmann R., Stuken A., Orr R.J., Svendsen H.M., Jakobsen K.S. Biosynthesis and molecular genetics of polyketides in marine dinoflagellates. Mar. Drugs 2010, 8:1011-1048.
25. Khosla C., Gokhale R.S., Jacobsen J.R., Cane D.E. Tolerance and specificity of polyketide synthases. Annu. Rev. Biochem. 1999, 68:219-253.
26. Lehane L., Lewis R.J. Ciguatera: recent advances but the risk remains. Int. J. Food Microbiol. 2000, 61:91-125.
27. Lewis R.J. Socioeconomic impacts and management of ciguatera in the Pacific. Bull. Soc. Pathol. Exot. 1992, 85:427-434.
28. Lidie K.B., Ryan J.C., Barbier M., 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. 2005, 7:481-493.
29. Lidie K.B., Van Dolah F.M. Spliced leader RNA-mediated trans-splicing in a dinoflagellate Karenia brevis. J. Eukaryot. Microbiol. 2007, 54(5):427-435.
30. Lin S., Zhang H., Zhuang Y., Tran B., Gill J. Spliced leader-based metatranscriptomic analysis lead to recognition of hidden genomic features in dinoflagellates. Proc. Natl. Acad. Sci. 2010, 107(46):20033-20038.
31. Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Lu F., Marchler G.H., Mullokandov M., Omelchenko M.V., Robertson C.L., Song J.S., Thanki N., Yamashita R.A., Zhang D., Zhang N., Zheng C., Bryant S.H. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 2011, 39:D225-D229.
32. McEwan M., Humayun R., Slamovits C.H., Keeling P.J. Nuclear genome sequence survey of the dinoflagellate Heterocapsa triquetra. J. Eukaryot. Microbiol. 2008, 55(6):530-535.
33. Monroe E.A., Johnson J.G., Wang Z., Pierce R.K., Van Dolah F.M. Characterization and expression of nuclear-encoded polyketide synthases in the brevetoxin-producing dinoflagellate Karenia brevis. J. Phycol. 2010, 46:541-552.
34. Monroe E.A., Van Dolah F.M. The toxic dinoflagellate Karenia brevis encodes novel type I-like polyketide synthases containing discrete catalytic domains. Protist 2008, 159:471-482.
35. Moulignier A., Binet D., Frottier J. Ciguatera fish poisoning: also in Europe. J. Neurol. Neurosurg. Psychiatry 1995, 59:192-199.
36. Otero P., Pérez S., Alfonso A., Vale C., Rodriguez P., Gouveia N.N., Gouveia N., Delgado J., Vale P., Hirama M., Ishihara Y., Molgo J., Botana L.M. First toxin profile of ciguateric fish in Madeira arquipelago (Europe). Anal. Chem. 2010, 82(14):6032-6039.
37. Pawlowiez R., Darius H.T., Cruchet P., Rossi F., Caillaud A., Laurent D., Chinain M. Evaluation of seafood toxicity in the Australes archipelago (French Polynesia) using the neuroblastoma cell-based assay. Food. Addit. Contam. A 2013, 30(3):567-586.
38. Ragelis E.P. Ciguatera seafood poisoning: overview. Seafood Toxins 1984, 25-36. American Chemical Society, Washington, DC. E.P. Ragelis (Ed.).
39. Rein K.S., Borrone J. Polyketides from dinoflagellates: origins, pharmacology and biosynthesis. Comp. Biochem. Physiol. B 1999, 124:117-131.
40. Rein K.S., Snyder R.V. The biosynthesis of polyketide metabolites by dinoflagellates. Adv. Appl. Microbiol. 2006, 59:93-125.
41. Shen B. Polyketide biosynthesis beyond the type I, II, and III polyketides synthase paradigms. Curr. Opin. Chem. Biol. 2003, 7:285-295.
42. Shimizu Y. Microalgal metabolites. Curr. Opin. Microbiol. 2003, 6:236-243.
43. Sonnenborn U., Kunau W.-H. Purification and properties of the fatty acid synthetase complex from the marine dinoflagellate, Crypthecodinium cohnii. Biochim. Biophys. Acta 1982, 712:523-534.
44. Staunton J., Weissman K.J. Polyketide biosynthesis: a millennium review. Nat. Prod. Rep. 2001, 18:380-416.
45. Stucken A., Orr R.J.S., Kellman R., Murray S.A., Neilan B.A., Jakobson K.S. Discovery of nuclear-encoded genes for the neurotoxin saxitoxin in dinoflagellates. PLoS ONE 2011, 6:e20096.
46. Tosteson T.R., Ballantine D.L., Tosteson C.G., Hensley V., Bardales A.T. Benthic dinoflagellate Ostreopsis lenticularis and Gambierdiscus toxicus. Appl. Environ. Microbiol. 1989, 55(1):137-141.
47. Van Dolah F.M., Zippay M., Pezzolesi L., Rein K., Johnson J.G., Wang Z., Pistocchi R. Subcellular localization of polyketide synthases and fatty acid synthase activity in dinoflagellates. J. Phycol. 2013, 10.1111/jpy.12120.
48. Weissman K.J. Polyketide biosynthesis: understanding and exploiting modularity. Philos. Trans. A: Math. Phys. Eng. Sci. 2004, 362:2671-2690.
49. Wisecaver J.H., Hackett J.D. Transcriptomic analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata. BMC Genomics 2010, 11:366.
50. Yamashita S., Ishihara Y., Morita H., Uchiyama J., Takeuchi K., Inoue M., Hirama M. Stereoselective 6-exo radical cyclization using cis-vinyl sulfoxide: practical total synthesis of CTX-3C. J. Nat. Prod. 2011, 74:357-364.
51. Yasumoto T., Nakajima I., Bagnis R., Adachi R. Finding of a dinoflagellate as a likely culprit of ciguatera. Bull. Jpn. Soc. Sci. Fish. 1977, 43:1021-1026.
52. Zhang H., Campbell D.A., Sturm N.R., Lin S. Dinoflagellate spliced-leader RNA genes display a variety of sequences and genomic arrangements. Mol. Biol. Evol. 2009, 26(8):1757-1771.
53. Zhang H., Hou Y., Miranda L., Campbell D.A., Sturm N.R., Gaasterland T., Lin S. Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. 2007, 104(11):4618-4623.
54. Zhang H., Zhuang Y., Gill J., Lin S. Proof that dinoflagellate spliced leader (DinoSL) is a useful hook for fishing dinoflagellate transcripts from mixed microbial samples: Symbiodinium kawagutii as a case study. Protist 2013, 164:510-527.