Advertisement

Coral Reefs

, Volume 32, Issue 4, pp 923–934 | Cite as

Lipid biomarkers in Symbiodinium dinoflagellates: new indicators of thermal stress

  • J. Kneeland
  • K. HughenEmail author
  • J. Cervino
  • B. Hauff
  • T. Eglinton
Report

Abstract

Lipid content and fatty acid profiles of corals and their dinoflagellate endosymbionts are known to vary in response to high-temperature stress. To better understand the heat-stress response in these symbionts, we investigated cultures of Symbiodinium goreauii type C1 and Symbiodinium sp. clade subtype D1 grown under a range of temperatures and durations. The predominant lipids produced by Symbiodinium are palmitic (C16) and stearic (C18) saturated fatty acids and their unsaturated analogs, the polyunsaturated fatty acid docosahexaenoic acid (C22:6, n-3; DHA), and a variety of sterols. Prolonged exposure to high temperature causes the relative amount of unsaturated acids within the C18 fatty acids in Symbiodinium tissue to decrease. Thermal stress also causes a decrease in abundance of fatty acids relative to sterols, as well as the more specific ratio of DHA to an algal 4-methyl sterol. These shifts in fatty acid unsaturation and fatty acid-to-sterol ratios are common to both types C1 and D1, but the apparent thermal threshold of lipid changes is lower for type C1. This work indicates that ratios among free fatty acids and sterols in Symbiodinium can be used as sensitive indicators of thermal stress. If the Symbiodinium lipid stress response is unchanged in hospite, the algal heat-stress biomarkers we have identified could be measured to detect thermal stress within the coral holobiont. These results provide new insights into the potential role of lipids in the overall Symbiodinium thermal stress response.

Keywords

Lipid biomarkers Thermal stress Symbiodinium Fatty acid unsaturation Thermal sensitivity 

Notes

Acknowledgments

Daniel Montluçon and Nick Drenzek assisted with lipid analyses. This research was supported by Award No. USA 00002 to K. Hughen made by King Abdullah University of Science and Technology (KAUST). This manuscript benefitted significantly from the helpful comments of two anonymous reviewers.

Supplementary material

338_2013_1076_MOESM1_ESM.doc (26 kb)
Supplementary material 1 (DOC 25 kb)
338_2013_1076_MOESM2_ESM.xls (100 kb)
Supplementary material 2 (XLS 99 kb)
338_2013_1076_MOESM3_ESM.xls (79 kb)
Supplementary material 3 (XLS 79 kb)

References

  1. Andrianasolo EH, Haramaty L, Vardi A, White E, Lutz R, Falkowski P (2008) Apoptosis-inducing galactolipids from a cultured marine diatom, Phaeodactylum tricornutum. J Nat Prod 71:1197–1201PubMedCrossRefGoogle Scholar
  2. Bachok Z, Mfilinge P, Tsuchiya M (2006) Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 25:545–554CrossRefGoogle Scholar
  3. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Syst 34:661–689CrossRefGoogle Scholar
  4. Black NA, Voellmy R, Szmant AM (1995) Heat shock protein induction in Montastraea faveolata and Aiptasia pallida exposed to elevated temperatures. Biol Bull 188:234–240CrossRefGoogle Scholar
  5. Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedCrossRefGoogle Scholar
  6. Borell EM, Bischof K (2008) Feeding sustains photosynthetic quantum yield of a scleractinian coral during thermal stress. Oecologia 157:593–601PubMedCrossRefGoogle Scholar
  7. Bouchard JN, Yamasaki H (2009) Implication of nitric oxide in the heat-stress-induced cell death of the symbiotic alga Symbiodinium microadriaticum. Mar Biol 156:2209–2220CrossRefGoogle Scholar
  8. Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reefs corals: evidence of photoinhibition and photoprotection. Coral Reefs 18:99–105CrossRefGoogle Scholar
  9. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism: a testable hypothesis. Bioscience 43:320–326CrossRefGoogle Scholar
  10. Catalá A (2009) Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem Phys Lipids 157:1–11PubMedCrossRefGoogle Scholar
  11. Cervino JM, Hayes R, Goreau TJ, Smith GW (2004) Zooxanthellae regulation in Yellow Blotch/Band and other coral diseases contrasted with temperature related bleaching: In situ destruction vs. expulsion. Symbiosis 37:63–85Google Scholar
  12. Cooper TF, Lai M, Ulstrup KE, Saunder SM, Flematti GR, Radford B, van Oppen MJH (2011) Symbiodinium genotypic and environmental controls on lipids in reef building corals. PLoS ONE 6(5):e20434. doi: 10.1371/journal.pone.0020434 PubMedCrossRefGoogle Scholar
  13. Díaz-Almeyda E, Thomé PE, El Hafidi M, Iglesias-Prieto R (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30:217–225CrossRefGoogle Scholar
  14. Douglas AE (2003) Coral bleaching – how and why? Mar Pollut Bull 46:385–392PubMedCrossRefGoogle Scholar
  15. Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G et al (2010) Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5(11):e13969. doi: 10.1371/journal.pone.0013969 PubMedCrossRefGoogle Scholar
  16. Eglinton TI, Eglinton G (2008) Molecular proxies for paleoclimatology. Earth Planet Sci Lett 275:1–16CrossRefGoogle Scholar
  17. Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65CrossRefGoogle Scholar
  18. Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: Implications for coral bleaching. Biol Bull 182:324–332CrossRefGoogle Scholar
  19. Gombos Z, Wada H, Hideg E, Murata N (1994) The unsaturation of membrane lipids stabilized photosynthesis against heat stress. Plant Physiol 104:563–567PubMedGoogle Scholar
  20. Goreau TJ, Hayes RL (1994) Coral bleaching and ocean “Hot Spots”. Ambio 23:176–180Google Scholar
  21. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631CrossRefGoogle Scholar
  22. Harroun TA, Katsaras J, Wassall SR (2008) Cholesterol is found to reside in the center of a polyunsaturated lipid membrane. Biochemistry 47:7090–7096PubMedCrossRefGoogle Scholar
  23. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofman EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases – Climate links and anthropogenic factors. Science 285:1505–1510PubMedCrossRefGoogle Scholar
  24. Hoegh-Guldberg O, Smith GJ (1989) The effects of sudden changes in light, temperature and salinity on the population density and export of zooxanthellae from the reef corals Seriatopora hystrix and Stylophora pistillata. J Exp Mar Biol Ecol 129:279–303CrossRefGoogle Scholar
  25. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305PubMedCrossRefGoogle Scholar
  26. Imbs AB, Demidkova DA, Dautova TN, Latyshev NA (2009) Fatty acid biomarkers of symbionts and unusual inhibition of tetracosapolyenoic acid biosynthesis in corals (Octocorallia). Lipids 44:325–335PubMedCrossRefGoogle Scholar
  27. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc B 275:1359–1365PubMedCrossRefGoogle Scholar
  28. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230Google Scholar
  29. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those in the Caribbean. Limnol Oceanogr 48:2046–2054CrossRefGoogle Scholar
  30. LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, López-Pérez A, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc R Soc B 277:2925–2934PubMedCrossRefGoogle Scholar
  31. LeBlond JD, Anderson B, Kofink D, Logares R, Rengefors K, Kremp A (2006) Fatty acid and sterol composition of two evolutionarily closely related dinoflagellate morphospecies from cold Scandinavian brackish and freshwaters. Eur J Phycol 41:303–311CrossRefGoogle Scholar
  32. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278PubMedCrossRefGoogle Scholar
  33. Mishra RK, Singhal GS (1992) Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids. Plant Physiol 98:1–6PubMedCrossRefGoogle Scholar
  34. Mostafavi PG, Fatemi SMR, Shahhosseiny MH, Hoegh-Guldberg O, Loh WKW (2007) Predominance of clade D Symbiodinium in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf, Iran). Mar Biol 153:25–34CrossRefGoogle Scholar
  35. Napolitano GE, Pollero RJ, Gayoso AM, Macdonald BA, Thompson RJ (1997) Fatty acids as trophic markers of photoplankton blooms in the Bahía Blanca Estuary (Buenos Aires, Argentina) and in Trinity Bay (Newfoundland, Canada). Biochem Syst Ecol 25:739–755CrossRefGoogle Scholar
  36. Oku H, Yamashiro H, Onaga K (2003) Lipid biosynthesis from [14C]-glucose in the coral Montipora digitata. Fish Sci 69:625–631CrossRefGoogle Scholar
  37. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958PubMedCrossRefGoogle Scholar
  38. Papina M, Meziane T, van Woesik R (2003) Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp Biochem Physiol B 135:533–537PubMedCrossRefGoogle Scholar
  39. Piorreck M, Pohl P (1984) Formation of biomass, total protein, chlorophylls, lipids, and fatty acids in green and blue-green algae during one growth phase. Phytochemistry 23:217–223CrossRefGoogle Scholar
  40. Pitman MC, Suits F, MacKerell AD Jr, Feller SE (2004) Molecular-level organization of saturated and polyunsaturated fatty acids in a phosphatidylcholine bilayer containing cholesterol. Biochemistry 43:15318–15328PubMedCrossRefGoogle Scholar
  41. Routaboul JM, Skidmore C, Wallis JG, Browse J (2012) Arabidopsis mutants reveal that short- and long-term thermotolerance have different requirements for trienoic fatty acids. J Exp Bot 63:1435–1443PubMedCrossRefGoogle Scholar
  42. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742PubMedCrossRefGoogle Scholar
  43. Stubbs CD, Smith AD (1984) The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 779:89–137PubMedCrossRefGoogle Scholar
  44. Suharsono BrownBE (1992) Comparative measurements of mitotic index in zooxanthellae from a symbiotic cnidarian subject to temperature increase. J Exp Mar Biol Ecol 158:179–188CrossRefGoogle Scholar
  45. Sutherland KP, Porter JW, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–309CrossRefGoogle Scholar
  46. Takahashi S, Whitney SM, Badger MA (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci USA 106:3237–3242PubMedCrossRefGoogle Scholar
  47. Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, Milligan AJ, Häggblom M, Falkowski PG, Field CB (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535PubMedCrossRefGoogle Scholar
  48. Tchernov D, Kvitt H, Haramaty L, Bibbyd TS, Gorbunov MY, Rosenfeld H, Falkowski PG (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci USA 108:9905–9909PubMedCrossRefGoogle Scholar
  49. Tolosa I, Treignier C, Grover R, Ferrier-Pagès C (2011) 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 30:763–774CrossRefGoogle Scholar
  50. Treignier C, Grover R, Ferrier-Pagès C, Tolosa I (2008) 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 53:2702–2710CrossRefGoogle Scholar
  51. Vidal-Dupiol J, Adjeroud M, Roger E, Foure L, Duval D, Mone Y, Ferrier-Pages C, Tambutte E, Tambutte S, Zoccola D, Allemand D, Mitta G (2009) Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BioMed Central Physiology 9:14PubMedGoogle Scholar
  52. Volkman JK (2003) Sterols in microorganisms. Appl Microbiol Biotechnol 60:4950506Google Scholar
  53. Volkman JK, Barrett SM, Blackburn SI, Mansour MP, Sikes EL, Gelin F (1998) Microalgal biomarkers: A review of recent research developments. Org Geochem 29:1163–1179CrossRefGoogle Scholar
  54. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012PubMedCrossRefGoogle Scholar
  55. Wilkinson C (ed) (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Center, Townsville, p 296Google Scholar
  56. Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids fatty acids and sterols in Okinawan corals. Comp Biochem Physiol B 122:397–407CrossRefGoogle Scholar
  57. Zhukova NV, Titlyanov EA (2003) Fatty acid variations in symbiotic dinoflagellates from Okinawan corals. Phytochemistry 62:191–195PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • J. Kneeland
    • 1
  • K. Hughen
    • 1
    Email author
  • J. Cervino
    • 1
  • B. Hauff
    • 2
  • T. Eglinton
    • 1
    • 3
  1. 1.Department of Marine Chemistry and GeochemistryWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Department of ZoologyMichigan State UniversityEast LansingUSA
  3. 3.Geological InstituteEidgenössische Technische HochschuleZurichSwitzerland

Personalised recommendations