Nutritional input from dinoflagellate symbionts in reef-building corals is minimal during planula larval life stage

Science Advances

Volumn 2, Issue 3, 2016, Pages

  Kopp, Christophe ^a   Domart Coulon, Isabelle ^b   Barthelemy, Dominique ^c   Meibom, Anders ^a,d  

^a EPFL   (Switzerland)

^b SORBONNE UNIVERSITÉ   (France)

^c Aquarium D'Océanopolis   (France)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CLIMATE CHANGE; MARINE BIOLOGY; REEFS; WATER ANALYSIS;

CELLULAR PROCESS; ENDOSYMBIOTIC; MARINE ORGANISMS; METABOLIC INTERACTIONS; METABOLIC SHIFT; SUB-CELLULAR; SYMBIOTIC PARTNERS; TRIGGER AND CONTROLS;

METABOLISM;

ANIMAL; ANTHOZOA; CLASSIFICATION; CORAL REEF; DINOFLAGELLATE; GENETICS; LARVA; MARINE BIOLOGY; NUTRITION; PHOTOSYNTHESIS; SYMBIOSIS;

ANIMALS; ANTHOZOA; CORAL REEFS; DINOFLAGELLIDA; LARVA; MARINE BIOLOGY; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PHOTOSYNTHESIS; SYMBIOSIS;

EID: 85019764111     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500681     Document Type: Article

References (34)

1. S. K. Davy, D. Allemand, V. M. Weis, Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76, 229-261 (2012).
2. P. L. Harrison, Coral Reefs: An Ecosystem in Transition (Springer, New York, 2011), pp. 59-85.
3. D. F. Gleason, D. K. Hofmann, Coral larvae: From gametes to recruits. J. Exp. Mar. Biol. Ecol. 408, 42-57 (2011).
4. R. H. Richmond, Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar. Biol. 93, 527-533 (1987).
5. S. Harii, K. Nadaoka, M. Yamamoto, K. Iwao, Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis. Mar. Ecol. Prog. Ser. 346, 89 (2007).
6. J. Figueiredo, A. H. Baird, M. F. Cohen, J.-F. Flot, T. Kamiki, T. Meziane, M. Tsuchiya, H. Yamasaki, Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs 31, 613-619 (2012).
7. E. M. Graham, A. H. Baird, S. R. Connolly, M. A. Sewell, B. L. Willis. Coral Reefs 32, 539-549 (2013).
8. M. R. Gaither, R. Rowan, Zooxanthellar symbiosis in planula larvae of the coral Pocillopora damicornis. J. Exp. Mar. Biol. Ecol. 386, 45-53 (2010).
9. R. H. Richmond, Energetic considerations in the dispersal of Pocillopora damicornis (Linnaeus) planulae, vol. 2 of Proceedings of the Fourth International Coral Reef Symposium, Manila, Philippines, 1981, vol. 2, pp. 153-156.
10. N. Isomura, M. Nishihira, Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals. Coral Reefs 20, 309-315 (2001).
11. S. Harii, M. Yamamoto, O. Hoegh-Guldberg, The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Mar. Biol. 157, 1215-1224 (2010).
12. R. Ben-David-Zaslow, Y. Benayahu, Competence and longevity in planulae of several species of soft corals. Mar. Ecol. Prog. Ser. 163, 235-243 (1998).
13. J. E. Parkinson, I. Baums, The extended phenotypes of marine symbioses: Ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front. Microbiol. 5, 445 (2014).
14. J.-F. Flot, H. Magalon, C. Cruaud, A. Couloux, S. Tillier, Patterns of genetic structure among Hawaiian corals of the genus Pocillopora yield clusters of individuals that are compatible with morphology. C. R. Biol. 331, 239-247 (2008).
15. S. Schmidt-Roach, P. Lundgren, K. J. Miller, G. Gerlach, A. M. E. Noreen, N. Andreakis, Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32, 161-172 (2013).
16. S. Schmidt-Roach, K. Miller, P. Lundgren, N. Andreakis, With eyes wide open: A revision of species within and closely related to the Pocillopora damicornis species complex (Scleractinia; Pocilloporidae) using morphology and genetics. Zool. J. Linn. Soc. 170, 1-33 (2014).
17. R. H. Richmond, P. L. Jokiel, Lunar periodicity in larva release in the reef coral Pocillopora damicornis at Enewetak and Hawaii. B. Mar. Sci. 34, 280-287 (1984).
18. T. C. LaJeunesse, 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 (2001).
19. M. Stat, X. Pochon, R. O. M. Cowie, R. D. Gates, Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar. Ecol. Prog. Ser. 386, 83-96 (2009).
20. C. Lechene, F. Hillion, G. McMahon, D. Benson, A. M. Kleinfeld, J. P. Kampf, D. Distel, Y. Luyten, J. Bonventre, D. Hentschel, K. M. Park, S. Ito, M. Schwartz, G. Benichou, G. Slodzian, High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. J. Biol. 5, 20 (2006).
21. P. Hoppe, S. Cohen, A. Meibom, NanoSIMS: Technical aspects and applications in cosmochemistry and biological geochemistry. Geostand. Geoanal. Res. 37, 111-154 (2013).
22. C. Kopp, I. Domart-Coulon, S. Escrig, B. M. Humbel, M. Hignetted, A. Meibom, Subcellular investigation of photosynthesis-driven carbon assimilation in the symbiotic reef coral Pocillopora damicornis. MBio 6, e02299-14 (2015).
23. C. Kopp, M. Pernice, I. Domart-Coulon, C. Djediat, J. E. Spangenberg, D. T. L. Alexander, M. Hignette, T. Meziane, A. Meibom, Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. MBio 4, e00052-13 (2013).
24. M. Pernice, A. Meibom, A. Van Den Heuvel, C. Kopp, I. Domart-Coulon, O. Hoegh-Guldberg, S. Dove, A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis. ISME J. 6, 1314-1324 (2012).
25. J. H. Vandermeulen, Studies on reef corals. II. Fine structure of planktonic planula larva of Pocillopora damicornis, with emphasis on the aboral epidermis. Mar. Biol. 27, 239-249 (1974).
26. J. Patton, S. Abraham, A. A. Benson, Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: Evidence for a light-driven carbon cycle between symbiont and host. Mar. Biol. 44, 235 (1977).
27. R. B. Kellogg, J. S. Patton, Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: A model coral polyp. Mar. Biol. 75, 137-149 (1983).
28. J. S. Patton, J. E. Burris, Lipid synthesis and extrusion by freshly isolated zooxanthellae (symbiotic algae). Mar. Biol. 75, 131-136 (1983).
29. C. J. Crossland, D. J. Barnes, M. A. Borowitzka, Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar. Biol. 60, 81-90 (1980).
30. R. Grover, J.-F. Maguer, D. Allemand, C. Ferrier-Pagès, Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J. Exp. Biol. 211, 860-865 (2008).
31. A. Apprill, H. Q. Marlow, M. Q. Martindale, M. S. Rappé, Specificity of associations between bacteria and the coral Pocillopora meandrina during early development. Appl. Environ. Microbiol. 78, 7467-7475 (2012).
32. J. L. Padilla-Gamiño, R. R. Bidigare, D. J. Barshis, A. Alamaru, L. Hédouin, X. Hernández-Pech, F. Kandel, S. L. Soon, M. S. Roth, L. J. Rodrigues, A. G. Grottoli, C. Portocarrero, S. A. Wagenhauser, F. Buttler, R. D. Gates, Are all eggs created equal? A case study from the Hawaiian reef-building coral Montipora capitata. Coral Reefs 32, 137-152 (2013).
33. P. J. Harrison, R. E. Waters, F. J. R. Taylor, A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. J. Phycol. 16, 28-35 (1980).
34. W. Loh, M. Hidaka, M. Hirose, E. A. Titlyanov, Genotypic diversity of symbiotic dinoflagellates associated with hermatypic corals from a fringing reef at Sesoko Island, Okinawa. J. Jpn. Coral Reef Soc. 2002, 1-9 (2002).