Differential distribution of lipids in epidermis, gastrodermis and hosted Symbiodinium in the sea anemone Anemonia viridis

Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology

Volumn 191, Issue , 2016, Pages 140-151

  Revel, Johana ^a,b,c   Massi, Lionel ^a,c   Mehiri, Mohamed ^a,c   Boutoute, Marc ^b,c   Mayzaud, Patrick ^b,c   Capron, Laure ^a,c   Sabourault, Cécile ^a,b,c  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CNRS   (France)

Author keywords

Anemonia; Cnidarian bleaching; Hyperthermal stress; Lipidomics; Symbiodinium; Symbiotic interaction

Indexed keywords

BIOLOGICAL MARKER; FATTY ACID; LIPID; STEROL; UNSATURATED FATTY ACID;

ANEMONIA VIRIDIS; ANIMAL TISSUE; ARTICLE; BLEACHING; CNIDARIA; CONTROLLED STUDY; ENDOSYMBIONT; EPIDERMIS; FATTY ACID ANALYSIS; GASTRODERMIS; HOST CELL; LIPID COMPOSITION; LIPID METABOLISM; MASS SPECTROMETRY; NONHUMAN; NUTRIENT CYCLING; REGULATORY MECHANISM; SEA ANEMONE; SYMBIODINIUM; SYMBIOSIS; TEMPERATURE STRESS; ANIMAL; CLUSTER ANALYSIS; DINOFLAGELLATE; HEAT SHOCK RESPONSE; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; CLUSTER ANALYSIS; DINOFLAGELLIDA; EPIDERMIS; FATTY ACIDS; HEAT-SHOCK RESPONSE; LIPID METABOLISM; SEA ANEMONES; STRESS, PHYSIOLOGICAL; SYMBIOSIS;

EID: 84945265060     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2015.10.017     Document Type: Article

References (92)

1. Ackman R. Flame ionization detection applied to thin-layer chromatography on coated quartz rods. Methods Enzymol. 1981, 72:205-252.
2. Al-Moghrabi S., Allemand D., Couret J.M., Jaubert J. Fatty acids of the scleractinian coral Galaxea fascicularis: effect of light and feeding. J. Comp. Physiol. B. 1995, 165:183-192.
3. Bachok Z., Mfilinge P., Tsuchiya M. Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 2006, 25:545-554.
4. Baumgarten S., Simakov O., Esherick L.Y., Liew Y.J., Lehnert E.M., Michell C.T., Li Y., Hambleton E.A., Guse A., Oates M.E., Gough J., Weis V.M., Aranda M., Pringle J.R., Voolstra C.R. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc. Natl. Acad. Sci. U. S. A. 2015, 10.1073/pnas.1513318112.
5. Benzécri J.P. L'analyse des données 1973, Tome 2 Dunod, Paris.
6. Bergé J.-P., Barnathan G. Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Advances in Biochemical Engineering/Biotechnology 2005, 96:49-125. Springer, Berlin Heidelberg. R. Ulber, Y. Gal (Eds.).
7. Bishop D., Kenrick J. Fatty acid composition of symbiotic zooxanthellae in relation to their hosts. Lipids 1980, 15:799-804. 10.1007/BF02534368.
8. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37:911-917.
9. Boutry J., Saliot A., Barbier M. The diversity of marine sterols and the role of algal bio-masses; from facts to hypothesis. Experientia 1979, 35:1541-1543.
10. Bythell J.C., Wild C. Biology and ecology of coral mucus release. J. Exp. Mar. Biol. Ecol. 2011, 408:88-93.
11. Casado-Amezúa P., Machordom A., Bernardo J., González-Wangüemert M. New insights into the genetic diversity of zooxanthellae in Mediterranean anthozoans. Symbiosis 2014, 63:41-46.
12. Christie W. The Analysis of Complex Lipids 1982, Pergamon Press, New York.
13. Clarke K., Green R. Statistical design and analysis for a 'biologicaleffects' study. Mar. Ecol. Prog. Ser. 1988, 46:213-226.
14. Crossland C.J., Barnes D.J., Cox T., Devereux M. Compartmentation and turnover of organic carbon in the Staghorn coral. Acropora formosa Mar. Biol. 1980, 59:181-187. 10.1007/BF00396866.
15. Dani V., Ganot P., Priouzeau F., Furla P., Sabourault C. Are Niemann-Pick type C proteins key players in cnidarian-dinoflagellate endosymbioses?. Mol. Ecol. 2014, 23:4527-4540.
16. Davy S.K., Allemand D., Weis V.M. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 2012, 76:229-261.
17. Downs C.A., Fauth J.E., Halas J.C., Dustan P., Bemiss J., Woodley C.M. Oxidative stress and seasonal coral bleaching. Free Radic. Biol. Med. 2002, 33:533-543.
18. Dubois N., Barnathan G., Gouygou J.-P., Bergé J.-P. Gas chromatographic behavior of fatty acid derivatives for mass spectrometry on low-polarity capillary columns. Eur. J. Lipid Sci. Technol. 2009, 111:688-697.
19. Dunn S.R., Thomas M.C., Nette G.W., Dove S.G. A lipidomic approach to understanding free fatty acid lipogenesis derived from dissolved inorganic carbon within cnidarian-dinoflagellate symbiosis. PLoS One 2012, 7.
20. Figueiredo J., Baird A.H., Cohen M.F., Flot J.F., Kamiki T., Meziane T., Tsuchiya M., Yamasaki H. Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 2012, 31:613-619.
21. Fitt W.K., Pardy R.L., Littler M.M. Photosynthesis, respiration, and contribution to community productivity of the symbiotic sea anemone Anthopleura elegantissima (Brandt, 1835). J. Exp. Mar. Biol. Ecol. 1982, 61:213-232.
22. Furla P., Bénazet-Tambutté S., Jaubert J., Allemand D. Functional polarity of the tentacle of the sea anemone Anemonia viridis: role in inorganic carbon acquisition. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1998, 274:R303-R310.
23. Ganot P., Moya A., Magnone V., Allemand D., Furla P., Sabourault C. Adaptations to endosymbiosis in a cnidarian-dinoflagellate association: differential gene expression and specific gene duplications. PLoS Genet. 2011, 7.
24. Garrabou J., Coma R., Bensoussan N., Bally M., Chevaldonné P., Cigliano M., Díaz D., Harmelin J.-G., Gambi M., Kersting D. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob. Chang. Biol. 2009, 15:1090-1103.
25. Garrett T.A., Schmeitzel J.L., Klein J.A., Hwang J.J., Schwarz J.A. Comparative lipid profiling of the cnidarian Aiptasia pallida and its dinoflagellate symbiont. PLoS One 2013, 8.
26. Gates R.D., Hoegh-Guldberg O., McFall-Ngai M.J., Bil K.Y., Muscatine L. Free amino acids exhibit anthozoan "host factor" activity: they induce the release of photosynthate from symbiotic dinoflagellates in vitro. Proc. Natl. Acad. Sci. 1995, 92:7430-7434.
27. Ghioni C., Porter A.E.A., Sadler I.H., Tocher D.R., Sargent J.R. Cultured fish cells metabolize octadecapentaenoic acid (all-cis δ3,6,9,12,15-18:5) to octadecatetraenoic acid (all-cis δ6,9,12,15-18:4) via its 2-trans intermediate (trans δ2, all-cis δ6,9,12,15-18:5). Lipids 2001, 36:145-153.
28. Grover R., Maguer J.-F., Reynaud-Vaganay S., Ferrier-Pages C. Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol. Oceanogr. 2002, 47:782-790.
29. Harland A.D., Fixter L.M., Davies P.S., Anderson R.A. Distribution of lipids between the zooxanthellae and animal compartment in the symbiotic sea anemone Anemonia viridis: wax esters, triglycerides and fatty acids. Mar. Biol. 1991, 110:13-19.
30. Harland A.D., Navarro J.C., Spencer Davies P., Fixter L.M. Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar. Biol. 1993, 117:113-117.
31. Hiraga Y., Shikano T., Widianti T., Ohkata K. Three new glycolipids with cytolytic activity from cultured marine dinoflagellate Heterocapsa circularisquama. Nat. Prod. Res. 2008, 22:649-657.
32. Hoegh-Guldberg O., Mumby P.J., Hooten A.J., Steneck R.S., Greenfield P., Gomez E., Harvell C.D., Sale P.F., Edwards A.J., Caldeira K., Knowlton N., Eakin C.M., Iglesias-Prieto R., Muthiga N., Bradbury R.H., Dubi A., Hatziolos M.E. Coral reefs under rapid climate change and ocean acidification. Science 2007, 318:1737-1742.
33. Imbs A., Demina O., Demidkova D. Lipid class and fatty acid composition of the boreal soft coral Gersemia rubiformis. Lipids 2006, 41:721-725.
34. Imbs A., Demidkova D., Dautova T., Latyshev N. Fatty acid biomarkers of symbionts and unusual inhibition of tetracosapolyenoic acid biosynthesis in corals (Octocorallia). Lipids 2009, 44:25-335. 10.1007/s11745-008-3266-2.
35. Imbs A., Yakovleva I., Latyshev N., Pham L. Biosynthesis of polyunsaturated fatty acids in zooxanthellae and polyps of corals. Russ. J. Mar. Biol. 2010, 36:452-457.
36. Imbs A.B., Latyshev N.A., Dautova T.N., Latypov Y.Y. Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae. Mar. Ecol. Prog. Ser. 2010, 409:65-75.
37. Imbs A., Yakovleva I. Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach. Coral Reefs 2012, 31:41-53.
38. Imbs A.B., Yakovleva I.M., Dautova T.N., Bui L.H., Jones P. Diversity of fatty acid composition of symbiotic dinoflagellates in corals: evidence for the transfer of host PUFAs to the symbionts. Phytochemistry 2014, 101:76-82.
39. Jeong H.J., Du Yoo Y., Kim J.S., Seong K.A., Kang N.S., Kim T.H. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci. J. 2010, 45:65-91.
40. Kaur G., Cameron-Smith D., Garg M., Sinclair A.J. Docosapentaenoic acid (22:5n-3): a review of its biological effects. Prog. Lipid Res. 2011, 50:28-34.
41. Kellogg R.B., Patton J.S. Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: a model coral polyp. Mar. Biol. 1983, 75:137-149.
42. Kneeland J., Hughen K., Cervino J., Hauff B., Eglinton T. Lipid biomarkers in Symbiodinium dinoflagellates: new indicators of thermal stress. Coral Reefs 2013, 32:923-934.
43. Kopp C., et al. MALDI-MS and NanoSIMS imaging techniques to study cnidarian-dinoflagellate symbioses. Zoology 2015, 118(2):125-131.
44. Lê S., Josse J., Husson F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 2008, 25:1-18.
45. LeBlanc D.C. Statistics: Concepts and Applications for Science 2004, Jones & Bartlett Learning.
46. Leblond J.D., Chapman P.J. Lipid class distribution of highly unsaturated long chain fatty acids in marine dinoflagellates. J. Phycol. 2000, 36:1103-1108.
47. Lehnert E.M., Mouchka M.E., Burriesci M.S., Gallo N.D., Schwarz J.A., Pringle J.R. Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians. G3: Genes|Genomes|Genetics 2014, 4:277-295.
48. Linebach J.A., Tesch B.P., Kovacsiss L.M. Nonparametric Statistics for Applied Research 2014, Springer.
49. Luo Y.-J., Wang L.H., Chen W.N., Peng S.E., Tzen J.C., Hsiao Y.Y., Huang H.J., Fang L.S., Chen C.S. Ratiometric imaging of gastrodermal lipid bodies in coral-dinoflagellate endosymbiosis. Coral Reefs 2009, 28:289-301.
50. Mansour M.P., Volkman J.K., Jackson A.E., Blackburn S.I. The fatty acid and sterol composition of five marine dinoflagellates. J. Phycol. 1999, 35:710-720.
51. Mansour M.P., Volkman J.K., Blackburn S.I. The effect of growth phase on the lipid class, fatty acid and sterol composition in the marine dinoflagellate, Gymnodinium sp. in batch culture. Phytochemistry 2003, 63:145-153. 10.1016/S0031-9422(03)00052-9.
52. Miller C.B., Morgan C.A., Prahl F., Sparrow M.A. Storage lipids of the copepod Calanus finmarchicus from Georges Bank and the Gulf of Maine. Limnol. Oceanogr. 1998, 43:488-497.
53. Miyazaki M., Ntambi J.M. Chapter 7 - fatty acid desaturation and chain elongation in mammals. Biochemistry of Lipids, Lipoproteins and Membranes (Fifth Edition) 2008, 191. Elsevier, San Diego. D.E. Vance, J.E. Vance (Eds.).
54. Miyazaki M., Kim H.-J., Man W.C., Ntambi J.M. Oleoyl-CoA is the major de novo product of stearoyl-CoA desaturase 1 gene isoform and substrate for the biosynthesis of the Harderian gland 1-alkyl-2,3-diacylglycerol. J. Biol. Chem. 2001, 276:39455-39461.
55. Morrison W.R., Smith L.M. Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J. Lipid Res. 1964, 5:600-608.
56. Moya A., Ganot P., Furla P., Sabourault C. The transcriptomic response to thermal stress is immediate, transient and potentiated by ultraviolet radiation in the sea anemone Anemonia viridis. Mol. Ecol. 2012, 21:1158-1174. 10.1111/j.1365-294X.2012.05458.x.
57. Muller-Parker G., Cook C., D'Elia C. Feeding affects phosphate fluxes in the symbiotic sea anemone Aiptasia pallida. Mar. Ecol. Prog. Ser. 1990, 60:283-290.
58. Murakami Y., Tsuyama M., Kobayashi Y., Kodama H., Iba K. Trienoic fatty acids and plant tolerance of high temperature. Sci. 2000, 287:476-479. 10.1126/science.287.5452.476.
59. Muscatine L. Glycerol excretion by symbiotic algae from corals and tridacna and its control by the host. Science 1967, 156:516-519.
60. Muscatine L., Cernichiari E. Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol. Bull. 1969, 137:506-523.
61. Nelson M., Phleger C., Mooney B., Nichols P. Lipids of gelatinous antarctic zooplankton: Cnidaria and Ctenophora. Lipids 2000, 35:551-559. 10.1007/s11745-000-555-5.
62. NIST/EPA/NIH mass spectral library, version 2.0f, build Oct 8 2008.
63. Oku H., Yamashiro H., Onaga K., Iwasaki H., Takara K. Lipid distribution in branching coral Montipora digitata. Fish. Sci. 2002, 68:517-522.
64. Papina M., Meziane T., van Woesik R. Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2003, 135:533-537.
65. Patton J., Burris J. Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar. Biol. 1983, 75:131-136.
66. Patton J., Abraham S., Benson A. Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle between symbiont and host. Mar. Biol. 1977, 44:235-247.
67. Peng S.-E., Chen W.-N.U., Chen H.-K., Lu C.-Y., Mayfield A.B., Fang L.-S., Chen C.-S. Lipid bodies in coral-dinoflagellate endosymbiosis: proteomic and ultrastructural studies. Proteomics 2011, 11:3540-3555.
68. Pernet V., Gavino V., Gavino G., Anctil M. Variations of lipid and fatty acid contents during the reproductive cycle of the anthozoan Renilla koellikeri. J. Comp. Physiol. B. 2002, 172:455-465. 10.1007/s00360-002-0268-x.
69. Pitman M.C., Suits F., MacKerell A.D., Feller S.E. Molecular-level organization of saturated and polyunsaturated fatty acids in a phosphatidylcholine bilayer containing cholesterol. Biochemistry 2004, 43:15318-15328.
70. Ramos R., González-Solís J. Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front. Ecol. Environ. 2012, 10:258-266.
71. Richier S., Furla P., Plantivaux A., Merle P.-L., Allemand D. Symbiosis-induced adaptation to oxidative stress. J. Exp. Biol. 2005, 208:277-285.
72. Sahu A., Jain D., Paliwal C., Ghosh T., Patidar S., Bhattacharya S., Mishra S. Fatty acids as biomarkers of microalgae. Phytochemistry 2013, 89:53-58.
73. Sargent J., Bell M., Henderson R., Tocher D. Polyunsaturated fatty acids in marine and terrestrial food webs. Animal Nutrition and Transport Processes 1990, 1:11-23.
74. Suzuki M., Watanabe K., Fujiwara S., Kurasawa T., Wakabayashi T., Tsuzuki M., Igguchi K., Yamori T. Isolation of peridinin-related norcarotenoids with cell growth-inhibitory activity from the cultured dinoflagellate of Symbiodinium sp., a symbiont of the Okinawan soft coral Clavularia viridis, and analysis of fatty acids of the dinoflagellate. Chem. Pharm. Bull. 2003, 51:724-727.
75. Tarrant A.M. Endocrine-like signaling in cnidarians: current understanding and implications for ecophysiology. Integr. Comp. Biol. 2005, 45:201-214.
76. Tarrant A.M., Reitzel A.M., Blomquist C.H., Haller F., Tokarz J., Adamski J. Steroid metabolism in cnidarians: insights from Nematostella vectensis. Mol. Cell. Endocrinol. 2009, 301:27-36.
77. Tchernov D., Gorbunov M.Y., de Vargas C., Narayan Yadav S., Milligan A.J., Häggblom M., Falkowski P.G. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:13531-13535.
78. Teece M.A., Estes B., Gelsleichter E., Lirman D. Heterotrophic and autotrophic assimilation of fatty acids by two scleractinian corals, Montastraea faveolata and Porites astreoides. Limnol. Oceanogr. 2011, 56:1285.
79. Tolosa I., Treignier C., Grover R., Ferrier-Pagès C. Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis. Coral Reefs 2011, 30:763-774.
80. Treignier C., Grove R., Ferrier-Pagès C., Tolosa I. Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol. Oceanogr. 2008, 2702-2710.
81. Treignier C., Tolosa I., Grover R., Reynaud S., Ferrier-Pagès C. Carbon isotope composition of fatty acids and sterols in the scleractinian coral Turbinaria reniformis: effect of light and feeding. Limnol. Oceanogr. 2009, 54:1933-1940.
82. Tytler E., Davies P.S. Photosynthetic production and respiratory energy expenditure in the anemone Anemonia sulcata (Pennant). J. Exp. Mar. Biol. Ecol. 1984, 81:73-86.
83. Visram S., Wiedenmann J., Douglas A. Molecular diversity of symbiotic algae of the genus Symbiodinium (Zooxanthellae) in cnidarians of the Mediterranean Sea. J. Mar. Biol. Assoc. U. K. 2006, 86:1281-1283.
84. Volkman J. Sterols in microorganisms. Appl. Microbiol. Biotechnol. 2003, 60:495-506.
85. Volkman J., Nichols P. Applications of thin layer chromatography-flame ionization detection to the analysis of lipids and pollutants in marine and environmental samples. J. Planar Chromatogr.-Mod. TLC 1991, 4:19-26.
86. Wakefield T., Farmer M., Kempf S. Revised description of the fine structure of in situ "zooxanthellae" genus Symbiodinium. Biol. Bull. 2000, 199:76-84.
87. Wang L.-H., Lee H.-H., Fang L.-S., Mayfield A.B., Chen C.-S. Fatty acid and phospholipid syntheses are prerequisites for the cell cycle of Symbiodinium and their endosymbiosis within sea anemones. PLoS One 2013, 8. 10.1371/journal.pone.0072486.
88. Weng L.-C., Pasaribu B., Ping Lin I., Tsai C.-H., Chen C.-S., Jiang P.-L. Nitrogen deprivation induces lipid droplet accumulation and alters fatty acid metabolism in symbiotic dinoflagellates isolated from Aiptasia pulchella. Sci. Rep. 2014, 4:5777.
89. Whitehead L., Douglas A. Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host. J. Exp. Biol. 2003, 206:3149-3157.
90. Yamashiro H., Oku H., Higa H., Chinen I., Sakai K. Composition of lipids, fatty acids and sterols in Okinawan corals. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 1999, 122:397-407.
91. Zeileis A., Wiel M.A., Hornik K., Hothorn T. Implementing a class of permutation tests: the coin package. J. Stat. Softw. 2008, 28:1-23.
92. Zhukova N.V., Titlyanov E.A. Fatty acid variations in symbiotic dinoflagellates from Okinawan corals. Phytochemistry 2003, 62:191-195.