Comparative Lipid Profiling of the Cnidarian Aiptasia pallida and Its Dinoflagellate Symbiont

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Garrett, Teresa A ^a   Schmeitzel, John L ^a   Klein, Joshua A ^a   Hwang, Janice J ^a   Schwarz, Jodi A ^a  

^a VASSAR COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDEAMINOETHYLPHOSPHONATE; GLYCEROPHOSPHOLIPID; LIPID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; SULFOQUINOVOSYLDIGLYCERIDE; UNCLASSIFIED DRUG;

AIPTASIA PALLIDA; ANIMAL TISSUE; ARTICLE; CNIDARIA; COLLISIONALLY ACTIVATED DISSOCIATION; CONTROLLED STUDY; DINOFLAGELLATE; ELECTROSPRAY MASS SPECTROMETRY; LIPIDOMICS; MASS SPECTROMETRY; NONHUMAN; QUADRUPOLE MASS SPECTROMETRY; SYMBIODINIUM; SYMBIONT; SYMBIOSIS; TIME OF FLIGHT MASS SPECTROMETRY;

ANIMALS; CNIDARIA; DINOFLAGELLIDA; LIPID METABOLISM; SYMBIOSIS;

EID: 84874642614     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057975     Document Type: Article

References (58)

1. Muscatine L, Falkowski PG, Dubinsky Z (1983) Carbon budgets in symbiotic associations. In: Schenk HEA, Schwemmler W, editors. Endocytobiology II. Intracellular Space as Oligogenetic Ecosystem. Berlin and New York: Walter de Gruyter. 649-673.
2. Davy SK, Allemand D, Weis VM, (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews 76: 229-261.
3. Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I, et al. (2012) A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME Journal 6: 1314-1324.
4. Wang JT, Douglas AE, (1998) Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis? Journal of Experimental Biology 201: 2445-2453.
5. Gates RD, Baghdasarian G, Muscatine L, (1992) Temperature stress causes host-cell detachment in symbiotic cnidarians-implications for coral bleaching. Biological Bulletin 182: 324-332.
6. Dunn SR, Schnitzler CE, Weis VM, (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: Every which way you lose. Proceedings of the Royal Society B 274: 3079-3085.
7. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
8. Meyer E, Weis VM, (2012) Study of cnidarian-algal symbiosis in the "omics" age. Biological Bulletin 223: 44-65.
9. Fitt WK, Trench RK, (1983) Endocytosis of the symbiotic dinoflagellate Symbiodinium Microadriaticum freudenthal by endodermal cells of the scyphistomae of Cassiopeia xamachana and resistance of the algae to host digestion. Journal of Cell Science 64: 195-212.
10. Schwarz JA, Krupp DA, Weis VM, (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biological Bulletin 196: 70-79.
11. Wakefield TS, Kempf SC, (2001) Development of host- and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biological Bulletin 200: 127-143.
12. Chen M, Hong M, Huang Y, Liu M, Cheng Y, et al. (2005) ApRab11, a cnidarian homologue of the recycling regulatory protein Rab11, is involved in the establishment and maintenance of the Aiptasia-Symbiodinium endosymbiosis. Biochemical and Biophysical Research Communications 338: 1607-1616.
13. Peng S, Wang Y, Wang L, Chen W-U, Lu C, et al. (2010) Proteomic analysis of symbiosome membranes in cnidaria- dinoflagellate endosymbiosis. Proteomics 10: 1002-1016.
14. Peng S, Chen W-U, Chen H, Lu C, Mayfield AB, et al. (2011) Lipid bodies in coral-dinoflagellate endosymbiosis: Proteomic and ultrastructural studies. Proteomics 11: 3540-3555.
15. Yamashiro H, Oku H, Higa H, Chinen I, Sakai K, (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comparative Biochemistry and Physiology- B Biochemistry and Molecular Biology 122: 397-407.
16. Tchernov D, Gorbunov MY, De Vargas C, Yadav SN, Milligant AJ, et al. (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academy of Sciences of the United States of America 101: 13531-13535.
17. Luo Y, Wang L, Chen W-U, Peng S, Tzen JT, et al. (2009) Ratiometric imaging of gastrodermal lipid bodies in coral-dinoflagellate endosymbiosis. Coral Reefs 28: 289-301.
18. Martin S, Parton RG, (2006) Lipid droplets: A unified view of a dynamic organelle. Nature Review Molecular Cellular Biology 7: 373-378.
19. Weis VM, Davy SK, Hoegh-Guldberg O, Rodriquiez-Lanetty M, Pringle JR, (2008) Cell biology in model systems as the key to understanding corals. Trends in Ecology and Evolution 23: 369-376.
20. Sunagawa S, Wilson EC, Thaler M, Smith M, Caruso C, et al. (2009) Generation and analysis of transcriptomic resources for a model system on the rise: The sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10: 258.
21. Belda-Baillie CA, Baillie BK, Maruyama T, (2002) Specificity of a model cnidarian-dinoflagellate symbiosis. Biological Bulletin 202: 74-85.
22. Santos SR, Taylor DJ, Coffroth MA, (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. Journal of Phycology 37: 900-912.
23. Lehnert EM, Burriesci MS, Pringle JR (2012) Developing the anemone Aiptasia as a tractable model for cnidarian-dinoflagellate symbiosis: The transcriptome of aposymbiotic A. pallida. BMC Genomics 13: art. no.271.
24. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37: 911-917.
25. Zemski Berry KA, Murphy RC, (2004) Electrospray ionization tandem mass spectrometry of glycerophosphoethanolamine plasmalogen phospholipids. Journal of the American Society for Mass Spectrometry 15: 1499-1508.
26. Bulat E, Garrett TA (2011) The putative N-acylphosphatidylethanolamine synthase from Arabidopsis thaliana is a lysoglycerophospholipid acyltransferase. Journal of Biological Chemistry: 33819-31.
27. Tautenhahn R, Patti GJ, Rinehart D, Siuzdak G, (2012) XCMS online: A web-based platform to process untargeted metabolomic data. Analytical Chemistry 84: 5035-5039.
28. Tautenhahn R, Böttcher C, Neumann S, (2008) Highly sensitive feature detection for high resolution LC/MS. BMC Bioinformatics 9: 504-520.
29. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57: 289-300.
30. Hsu F, Turk J, (2009) Electrospray ionization with low-energy collisionally activated dissociation tandem mass spectrometry of glycerophospholipids: Mechanisms of fragmentation and structural characterization. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences 877: 2673-2695.
31. Hsu F, Turk J, (2000) Characterization of phosphatidylinositol, phosphatidylinositol-4-phosphate, and phosphatidylinositol-4,5-bisphosphate by electrospray ionization tandem mass spectrometry: A mechanistic study. Journal of the American Society for Mass Spectrometry 11: 986-999.
32. Pulfer M, Murphy RC, (2003) Electrospray mass spectrometry of phospholipids. Mass Spectrometry Reviews 22: 332-364.
33. Hsu F, Turk J, (2005) Studies on phosphatidylserine by tandem quadrupole and multiple stage quadrupole ion-trap mass spectrometry with electrospray ionization: Structural characterization and the fragmentation processes. Journal of the American Society for Mass Spectrometry 16: 1510-1522.
34. Fahy E, Subramaniam S, Brown HA, Glass CK, Merrill AHJ, et al. (2005) A comprehensive classification system for lipids. Journal of Lipid Research 46: 839-861.
35. de Souza LM, Iacomini M, Gorin PAJ, Sari RS, Haddad MA, et al. (2007) Glyco- and sphingophosphonolipids from the medusa Phyllorhiza punctata: NMR and ESI-MS/MS fingerprints. Chemistry and Physics of Lipids 145: 85-96.
36. Ren S, Hylemon P, Zhang Z, Rodriguez-Agudo D, Marques D, et al. (2006) Identification of a novel sulfonated oxysterol, 5-cholesten-3β,25-diol 3-sulfonate, in hepatocyte nuclei and mitochondria. Journal of Lipid Research 47: 1081-1090.
37. Zhang X, Fhaner CJ, Ferguson-Miller SM, Reid GE, (2012) Evaluation of ion activation strategies and mechanisms for the gas-phase fragmentation of sulfoquinovosyldiacylglycerol lipids from Rhodobacter sphaeroides. International Journal of Mass Spectrometry 316-318: 100-107.
38. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G, (2006) XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Analytical Chemistry 78: 779-787.
39. Rouser G, Kritchevsky G, Yamamoto AG, Simon G, (1968) Accumulation of a glycerophospholipid in a classical Niemann-Pick disease. Lipids 3: 287-290.
40. Zhukova NV, Titlyanov EA, (2003) Fatty acid variations in symbiotic dinoflagellates from Okinawan corals. Phytochemistry 62: 191-195.
41. Imbs AB, Latyshev NA, Zhukova NV, Dautova TN, (2007) Comparison of fatty acid compositions of azooxanthellate Dendronephthya and zooxanthellate soft coral species. Comparative Biochemistry and Physiology- B Biochemistry and Molecular Biology 148: 314-321.
42. Lin C, Wang L, Fan T, Kuo F, (2012) Lipid content and composition during the oocyte development of two gorgonian coral species in relation to low temperature preservation. PLoS ONE 7: e38698.
43. Shimojima M, (2011) Biosynthesis and functions of the plant sulfolipid. Progress in Lipid Research 50: 234-239.
44. Wang Z, Benning C, (2012) Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochemical Society Transactions 40: 457-463.
45. De Souza LM, Sassaki GL, Romanos MTV, Barreto-Bergter E, (2012) Structural characterization and anti-HSV-1 and HSV-2 activity of glycolipids from the marine algae Osmundaria obtusiloba isolated from southeastern Brazilian coast. Marine Drugs 10: 918-931.
46. Sprott GD, Larocque S, Cadotte N, Dicaire CJ, McGee M, et al. (2003) Novel polar lipids of halophilic eubacterium Planococcus H8 and archaeon Haloferax volcanii. Biochimica et Biophysica Acta- Molecular and Cell Biology of Lipids 1633: 179-188.
47. Cedergren RA, Hollingsworth RI, (1994) Occurrence of sulfoquinovosyl diacylglycerol in some members of the family Rhizobiaceae. Journal of Lipid Research 35: 1452-1461.
48. Langworthy TA, Mayberry WR, Smith PF, (1976) A sulfonolipid and novel glucosamidyl glycolipids from the extreme thermoacidophile Bacillus acidocaldarius. Biochimica et Biophysica Acta 431: 550-569.
49. Jones MR, (2007) Lipids in photosynthetic reaction centres: Structural roles and functional holes. Progress in Lipid Research 46: 56-87.
50. Leech RM, Rumsby MG, Thomson WW, (1973) Plastid differentiation, acyl lipid, and fatty acid changes in developing green maize leaves. Plant Physiology 52: 240-245.
51. Shibuya I, Hase E, (1965) Degradation and formation of sulfolipid occurring concurrently with de- and re-generation of chloroplasts in the cells of Chlorella protothecoides. Plant and Cell Physiology 6: 267-283.
52. Díaz-Almeyda E, Thomé PE, Hafidi ME, Iglesias-Prieto R, (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30: 217-225.
53. Burgos A, Szymanski J, Seiwert B, Degenkolbe T, Hannah MA, et al. (2011) Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light. Plant Journal 66: 656-668.
54. Awai K, Matsuoka R, Shioi Y (2012) Lipid and fatty acid compositions of Symbiodinium strains. Proceedings of the 12th International Coral Reef Symposium.
55. Yamada S, Araki S, Abe S, Kon K, Ando S, et al. (1995) Structural analysis of a novel triphosphonoglycosphingolipid from the egg of the sea hare, Aplysia kurodai. Journal of Biochemistry 117: 794-799.
56. Mukhamedova KS, Glushenkova AI, (2000) Natural phosphonolipids. Chemistry of Natural Compounds 36: 329-341.
57. Kononova SV, Nesmeyanova MA, (2002) Phosphonates and their degradation by microorganisms. Biochemistry (Moscow) 67: 184-195.
58. Chintalapati M, Truax R, Stout R, Portier R, Losso JN, (2009) In vitro and in vivo anti-angiogenic activities and inhibition of hormone-dependent and-independent breast cancer cells by ceramide methylaminoethylphosphonate. Journal of Agricultural and Food Chemistry 57: 5201-5210.