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Production of three symbiosis-related fatty acids by Symbiodinium types in clades A–F associated with marine invertebrate larvae

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Abstract

Symbiodinium are dinoflagellates engaged in a mutualistic symbiosis with multiple coral reef taxa. They are divided in nine different clades (A–I), which typically associate with different hosts. However, very little information is available on metabolic differences in Symbiodinium types, especially when associated with metazoan larvae. We tested whether three ω3 fatty acids (stearidonic acid, SDA; docosapentaenoic acid, DPA; and docosahexaenoic acid, DHA) that are typically translocated from Symbiodinium to its host are produced by Symbiodinium types within clades A–F associated with Mussismilia hispida (scleractinian coral), Berghia stephanieae (nudibranch), and Tridacna crocea (giant clam) larvae. We acquired and spawned broodstock for each host, cultured their larvae, and offered Symbiodinium types belonging to clades A–F. Samples were taken during a 72-h window after the offer of Symbiodinium, and fatty acids were extracted and analyzed by gas chromatography. The concentrations of SDA and DPA for all host larvae–dinoflagellate associations were low and variable, without trends. However, M. hispida planula larvae associated with Symbiodinium A1 and C1 had a statistically significant higher amount of DHA. The veliger larvae of B. stephanieae digested the Symbiodinium, and the amount of DHA remained constant throughout the experiment. The veliger larvae of T. crocea associated with Symbiodinium A1 and C1 also presented a higher amount of DHA, although not statistically different from the other types. These results show that Symbiodinium A1 and C1, in the case of M. hispida and T. crocea (which usually harbor strains within clades A and C), may contribute a small amount of DHA to the larvae of these organisms and form a stronger mutualism than other strains.

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References

  • Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941

    CAS  Google Scholar 

  • Arai I, Kato M, Heyward A, Ikeda Y, Iizuka T, Maruyama T (1993) Lipid composition of positively buoyant eggs of reef building corals. Coral Reefs 12:71–75

    Article  Google Scholar 

  • Bachok Z, Mfilinge P, Tsuchiya M (2006) Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 25:545–554

    Article  Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • Belda-Baillie CA, Baillie BK, Maruyama T (2002) Specificity of a model cnidarian–dinoflagellate symbiosis. Biol Bull 202:74–85

    Article  CAS  PubMed  Google Scholar 

  • Belda-Baillie CA, Sison M, Silvestre V, Villamor K, Monje V, Gomez ED, Baillie BK (1999) Evidence for changing symbiotic algae in juvenile tridacnids. J Exp Mar Bio Ecol 241:207–221

    Article  Google Scholar 

  • Bergé JP, Barnathan G (2005) Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Adv Biochem Eng Biotechnol 96:49–125

    PubMed  Google Scholar 

  • Braley RD (1985) Serotonin-induced spawning in giant clams (Bivalvia: Tridacnidae). Aquaculture 47:321–325

    Article  CAS  Google Scholar 

  • Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mamm Sci 22:759–801

    Article  Google Scholar 

  • Carlos AA, Baillie BK, Maruyama T (2000) Diversity of dinoflagellate symbionts (zooxanthellae) in a host individual. Mar Ecol Prog Ser 195:93–100

    Article  Google Scholar 

  • Carroll DJ, Kempf SC (1990) Laboratory culture of the aeolid nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia): some aspects of its development and life history. Biol Bull 179:243–253

    Article  Google Scholar 

  • Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34

    Article  CAS  PubMed  Google Scholar 

  • Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kühl M, Muirhead A, O’Leary RA, Ziersen BEF, van Oppen MJH (2011) Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc R Soc Lond B Biol Sci 278:1840–1850

    Article  Google Scholar 

  • Dalsgaard J, St John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340

    Article  PubMed  Google Scholar 

  • DeBoer TS, Baker AC, Erdmann MV, Ambariyanto Jones PR, Barber PH (2012) Patterns of Symbiodinium distribution in three giant clam species across the biodiverse Bird’s Head region of Indonesia. Mar Ecol Prog Ser 444:117–132

    Article  CAS  Google Scholar 

  • Figueiredo J, Baird AH, Cohen MF, Flot JF, Kamiki T, Meziane T, Tsuchiya M, Yamasaki H (2012) Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31:613–619

    Article  Google Scholar 

  • Fransolet D, Roberty S, Plumier JC (2012) Establishment of endosymbiosis: the case of cnidarians and Symbiodinium. J Exp Mar Bio Ecol 420–421:1–7

    Article  Google Scholar 

  • Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. Journal Protozool 9:45–52

    Article  Google Scholar 

  • Gordon BR, Leggat W (2010) Symbiodinium–invertebrate symbioses and the role of metabolomics. Mar Drugs 8:2546–2568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goulet TL (2006) Most corals may not change their symbionts. Mar Ecol Prog Ser 321:1–7

    Article  Google Scholar 

  • Graeve M, Kattner G, Hagen W (1994) Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: experimental evidence of trophic markers. J Exp Mar Bio Ecol 182:97–110

    Article  CAS  Google Scholar 

  • Grant AJ, Rémond M, People J, Hinde R (1997) Effects of host-tissue homogenate of the scleractinian coral Plesiastrea versipora on glycerol metabolism in isolated symbiotic dinoflagellates. Mar Biol 128:665–670

    Article  CAS  Google Scholar 

  • Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms, I: Cycotella nana Hustedt, and Detonula confervacea (CLEVE) Gran. Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Heslinga GA, Watson TC, Isamu T (1990) Giant clam farming. Pacific Fisheries Development Foundation (NMFS/NOAA), Honolulu

  • Hume BCC, D’Angelo C, Smith EG, Stevens JR, Burt J, Wiedenmann J (2015) Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci Rep 5:8562

  • Imbs AB, Demidkova DA, Latypov YY, Pham LQ (2007) Application of fatty acids for chemotaxonomy of reef-building corals. Lipids 42:1035–1046

    Article  CAS  PubMed  Google Scholar 

  • Imbs AB, Yakovleva IM, Dautova TN, Bui LH, Jones P (2014) Diversity of fatty acid composition of symbiotic dinoflagellates in corals: evidence for the transfer of host PUFAs to the symbionts. Phytochemistry 101:76–82

    Article  CAS  PubMed  Google Scholar 

  • Klueter A, Crandall J, Archer F, Teece M, Coffroth M (2015) Taxonomic and environmental variation of metabolite profiles in marine dinoflagellates of the genus Symbiodinium. Metabolites 5:74–99

    Article  PubMed  PubMed Central  Google Scholar 

  • Kneeland J, Hughen K, Cervino J, Hauff B, Eglinton T (2013) Lipid biomarkers in Symbiodinium dinoflagellates: new indicators of thermal stress. Coral Reefs 32:923–934

    Article  Google Scholar 

  • Kopp C, Domart-Coulon I, Barthelemy D, Meibom A (2016) Nutritional input from dinoflagellate symbionts in reef-building corals is minimal during planula larval life stage. Sci Adv 2:e1500681

    Article  PubMed  PubMed Central  Google Scholar 

  • Ladner JT, Barshis DJ, Palumbi SR (2012) Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol Biol 12:217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  • LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134

    Article  CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with Cnidaria. J Phycol 48:1380–1391

    Article  PubMed  Google Scholar 

  • LaJeunesse TC, Lee SY, Gil-Agudelo DL, Knowlton N, Jeong HJ (2015) Symbiodinium necroappetens sp. nov., (Dinophyceae): an opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals. Eur J Phycol 50:223–238

    Article  Google Scholar 

  • Leal MC, Nunes C, Alexandre D, da Silva TL, Reis A, Dinis MT, Calado R (2012) Parental diets determine the embryonic fatty acid profile of the tropical nudibranch Aeolidiella stephanieae: the effect of eating bleached anemones. Mar Biol 159:1745–1751

    Article  CAS  Google Scholar 

  • Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, LaJeunesse TC (2015) Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank. Eur J Phycol 50:155–172

    Article  Google Scholar 

  • Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

    Article  CAS  PubMed  Google Scholar 

  • Loh WKW, Cowlishaw M, Wilson NG (2006) Diversity of Symbiodinium dinoflagellate symbionts from the Indo-Pacific sea slug Pteraeolidia ianthina (Gastropoda: Mollusca). Mar Ecol Prog Ser 320:177–184

    Article  CAS  Google Scholar 

  • Mansour MP, Volkman JK, Jackson AE, Blackburn SI (1999) The fatty acid and sterol composition of two marine dinoflagellates. J Phycol 35:710–720

    Article  CAS  Google Scholar 

  • Masood A, Stark KD, Salem N Jr (2005) A simplified and efficient method for the analysis of fatty acid methyl esters suitable for large clinical studies. J Lipid Res 46:2299–2305

    Article  CAS  PubMed  Google Scholar 

  • Mies M, Braga F, Scozzafave MS, Lemos D, Sumida PYG (2012) Early development, survival and growth rates of the giant clam Tridacna crocea (Bivalvia: Tridacnidae). Braz J Oceanogr 60:129–135

    Article  Google Scholar 

  • Mies M, Braga F, Scozzafave MS, Sumida PYG, Lemos D (2013) Successful spawning and a possible solution for broodstock mortality in giant clams (Tridacnidae): a neurotransmitter injection through the byssal orifice. Aquac Res 44:671–676

    Article  CAS  Google Scholar 

  • Mies M, Sumida PYG, Rädecker N, Voolstra CR (2017a) Marine invertebrate larvae associated with Symbiodinium: a mutualism from the start? Front Ecol Evol 5:56

    Article  Google Scholar 

  • Mies M, Voolstra CR, Castro CB, Pires DO, Calderon EN, Sumida PYG (2017b) Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae. R Soc Open Sci 4:170253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mortillaro JM, Pitt KA, Lee SY, Meziane T (2009) Light intensity influences the production and translocation of fatty acids by zooxanthellae in the jellyfish Cassiopea sp. J Exp Mar Bio Ecol 378:22–30

    Article  CAS  Google Scholar 

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in coral reefs. In: Dubinsky Z (ed) Ecosystems of the world. Elsevier, Amsterdam, pp 75–87

    Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. BioScience 27:454–460

    Article  Google Scholar 

  • Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    Article  CAS  Google Scholar 

  • Nevejan N, Saez I, Gajardo G, Sorgeloos P (2003) Supplementation of EPA and DHA emulsions to a Dunaliella tertiolecta diet: effect on growth and lipid composition of scallop larvae, Argopecten purpuratus (Lamarck, 1819). Aquaculture 217:613–632

    Article  CAS  Google Scholar 

  • Neves EG, Pires DO (2002) Sexual reproduction of Brazilian coral Mussismilia hispida (Verrill, 1902). Coral Reefs 21:161–168

    Google Scholar 

  • Papina M, Meziane T, van Woesik R (2003) Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comp Biochem Physiol B 135:533–537

    Article  CAS  PubMed  Google Scholar 

  • Picciani N, Seiblitz IGL, de Paiva PC, Castro CB, Zilberberg C (2016) Geographic patterns of Symbiodinium diversity associated with the coral Mussismilia hispida (Cnidaria, Scleractinia) correlate with major reef regions in the southwestern Atlantic Ocean. Mar Biol 163:236

    Article  Google Scholar 

  • Pires DO, Castro CB, Segal B, Pereira CM, do Carmo EC, da Silva RG, Calderon EN (2016) Reprodução de corais de águas rasas do Brasil. In: Zilberberg C, Abrantes DP, Marques JA, Machado LF, Marangoni LFB (eds) Conhecendo os Recifes Brasileiros. Museu Nacional, Rio de Janeiro, pp 111–128

    Google Scholar 

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497

    Article  CAS  PubMed  Google Scholar 

  • Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Lanetty M, Chang SJ, Song JI (2003) Specificity of two temperate dinoflagellate–anthozoan associations from the north-western Pacific Ocean. Mar Biol 143:1193–1199

    Article  Google Scholar 

  • Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73

    Article  CAS  Google Scholar 

  • Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral–algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruess L, Tiunov A, Haubert D, Richnow HH, Häggblom MM, Scheu S (2005) Carbon stable isotope fractionation and trophic transfer of fatty acids in fungal based soil food chains. Soil Biol Biochem 37:945–953

    Article  CAS  Google Scholar 

  • Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (= Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proc R Soc Lond B Biol Sci 207:405–427

    Article  CAS  Google Scholar 

  • Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43

    Article  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trench RK (1979) The cell biology of plant–animal symbiosis. Annu Rev Plant Physiol 30:485–531

    Article  CAS  Google Scholar 

  • Trench RK, Wethey DS, Porter JW (1981) Observations on the symbiosis with zooxanthellae among the Tridacnidae (Mollusca, Bivalvia). Biol Bull 161:180–198

    Article  Google Scholar 

  • van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24:482–487

    Article  Google Scholar 

  • Venn AA, Loram JE, Douglas AE (2008) Photosynthetic symbioses in animals. J Exp Bot 59:1069–1080

    Article  CAS  PubMed  Google Scholar 

  • Volkman JK, Jeffrey SW, Nichols PD, Rogers GI, Garland CD (1989) Fatty acid and lipid composition of 10 species of microalgae used in mariculture. J Exp Mar Biol Ecol 128:219–240

    Article  CAS  Google Scholar 

  • Weis VM, Reynolds WS, DeBoer MD, Krupp DA (2001) Host–symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:301–308

    Article  Google Scholar 

  • Wilkerson FP (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009–1014

    Article  Google Scholar 

  • Zhukova N, Aizdaicher NA (1995) Fatty acid composition of 15 species of marine microalgae. Phytochemistry 39:351–356

    Article  CAS  Google Scholar 

  • Zhukova NV, Titlyanov EA (2003) Fatty acid variations in symbiotic dinoflagellates from Okinawan corals. Phytochemistry 62:191–195

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Mary Alice Coffroth for her comments on the manuscript and also for supplying the Symbiodinium cultures. We thank Carla Zilberberg and Ronaldo Francini-Filho for reviewing the manuscript and also Flávia Saldanha-Corrêa, the entire Coral Vivo Institute staff, Henrique Alves, Priscilla Derogis, and Linda Waters. This work was supported by Projeto Coral Vivo and sponsored by Petrobras and Arraial d’Ajuda Eco Parque. PYGS acknowledges Grants 302526/2012-9 and 2010/20350-8 from CNPq and FAPESP.

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  1. Oceanographic Institute, University of São Paulo, Praça do Oceanográfico, 191, São Paulo, SP, 05508-120, Brazil

    M. Mies, A. Z. Güth, A. A. Tenório & P. Y. G. Sumida

  2. Chemistry Institute, University of São Paulo, Av Prof Lineu Prestes, 748, São Paulo, SP, 05508-000, Brazil

    A. B. Chaves-Filho & S. Miyamoto

  3. Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, s/n, Rio de Janeiro, RJ, 20940-040, Brazil

    C. B. Castro & D. O. Pires

  4. Instituto Coral Vivo, Rua dos Coqueiros, 87, Santa Cruz Cabrália, BA, 45807-000, Brazil

    C. B. Castro, D. O. Pires & E. N. Calderon

  5. Núcleo em Ecologia e Desenvolvimento Socioambiental de Macaé, Universidade Federal do Rio de Janeiro, Av São José do Barreto, 764, Macaé, RJ, 27965-045, Brazil

    E. N. Calderon

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  1. M. Mies
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Mies, M., Chaves-Filho, A.B., Miyamoto, S. et al. Production of three symbiosis-related fatty acids by Symbiodinium types in clades A–F associated with marine invertebrate larvae. Coral Reefs 36, 1319–1328 (2017). https://doi.org/10.1007/s00338-017-1627-0

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