Table of Contents Author Guidelines Submit a Manuscript
Journal of Marine Biology
Volume 2017 (2017), Article ID 3130723, 7 pages
https://doi.org/10.1155/2017/3130723
Research Article

Experimentally Induced Bleaching in the Sea Anemone Exaiptasia Supports Glucose as a Main Metabolite Associated with Its Symbiosis

1Instituto Tecnológico de Morelia, Av. Tecnológico 15000, 58120 Morelia, MICH, Mexico
2Programa de Posgrado en Ciencias del Mar y Limnología, Mexico City, Mexico
3Unidad Académica de Sistemas Arrecifales Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apartado Postal 13, 77500 Cancún, QROO, Mexico

Correspondence should be addressed to Patricia Elena Thomé

Received 23 September 2017; Accepted 14 November 2017; Published 5 December 2017

Academic Editor: Horst Felbeck

Copyright © 2017 Víctor Hugo Molina et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Muscatine and J. W. Porter, “Reef corals: mutualistic symbioses adapted to nutrient-poor environments,” Bioscience, vol. 27, no. 7, pp. 454–460, 1977. View at Publisher · View at Google Scholar
  2. D. Yellowlees, T. A. V. Rees, and W. Leggat, “Metabolic interactions between algal symbionts and invertebrate hosts,” Plant, Cell & Environment, vol. 31, no. 5, pp. 679–694, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Muscatine, “Glycerol excretion by symbiotic algae from corals and Tridacna and its control by the host,” Science, vol. 156, no. 3774, pp. 516–519, 1967. View at Publisher · View at Google Scholar · View at Scopus
  4. R. K. Trench, “The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates. III. The effect of homogenates of host tissues on the excretion of photosynthetic products in vitro by zooxanthellae from two marine coelenterates,” Proceedings of the Royal Society B Biological Science, vol. 177, no. 1047, pp. 251–264, 1971. View at Publisher · View at Google Scholar
  5. K. Schmitz and B. P. Kremer, “Carbon fixation and analysis of assimilates in a coral-dinoflagellate symbiosis,” Marine Biology, vol. 42, no. 4, pp. 305–313, 1977. View at Publisher · View at Google Scholar · View at Scopus
  6. D. K. Hofmann and B. P. Kremer, “Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): Significance of endosymbiotic dinoflagellates,” Marine Biology, vol. 65, no. 1, pp. 25–33, 1981. View at Publisher · View at Google Scholar · View at Scopus
  7. J. F. Battey and J. S. Patton, “A reevaluation of the role of glycerol in carbon translocation in zooxanthellae-coelenterate symbiosis,” Marine Biology, vol. 79, no. 1, pp. 27–38, 1984. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Streamer, Y. McNeil, and D. Yellowlees, “The short-term partitioning of carbon-14 assimilate between zooxanthellae and polyp tissue in Acropora formosa,” Marine Biology, vol. 90, no. 4, pp. 565–573, 1986. View at Publisher · View at Google Scholar · View at Scopus
  9. D. H. Lewis and D. C. Smith, “The autotrophic nutrition of symbiotic marine coelenterates with special reference to.hermatypic corals. I. movement of photosynthetic products between the symbionts,” Proceedings of the Royal Society B Biological Science, vol. 178, no. 1050, pp. 111–129, 1971. View at Publisher · View at Google Scholar
  10. D. L. Taylor, “Nutrition of algal-invertebrate symbiosis. I. utilization of soluble organic nutrients by symbiont-free hosts,” Proceedings of the Royal Society B Biological Science, vol. 186, no. 1085, pp. 357–368, 1974. View at Publisher · View at Google Scholar · View at Scopus
  11. J.-P. Gattuso, D. Yellowlees, and M. Lesser, “Depth- and light-dependent variation of carbon partitioning and utilization in the zooxanthellate scleractinian coral Stylophora pistillata,” Marine Ecology Progress Series, vol. 92, no. 3, pp. 267–276, 1993. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Hagedorn, V. L. Carter, S. Ly et al., “Analysis of internal osmolality in developing coral larvae, fungia scutaria,” Physiological and Biochemical Zoology, vol. 83, no. 1, pp. 157–166, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. M. S. Burriesci, T. K. Raab, and J. R. Pringle, “Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis,” Journal of Experimental Biology, vol. 215, no. 19, pp. 3467–3477, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Davy and C. Cook, “The relationship between nutritional status and carbon flux in the zooxanthellate sea anemone Aiptasia pallida,” Marine Biology, vol. 139, no. 5, pp. 999–1005, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. C. B. Cook, C. F. D'Elia, and G. Muller-Parker, “Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida,” Marine Biology, vol. 98, no. 2, pp. 253–262, 1988. View at Publisher · View at Google Scholar · View at Scopus
  16. P. G. Falkowski, Z. Dubinsky, L. Muscatine, and L. McCloskey, “Population control in symbiotic corals: ammonium ions and organic materials maintain the density of zooxanthellae,” Bioscience, vol. 43, no. 9, pp. 606–611, 1993. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Grover, J.-F. Maguer, S. Reynaud-Vaganay, and C. Ferrier-Pagès, “Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations,” Limnology and Oceanography, vol. 47, no. 3, pp. 782–790, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Ezzat, J.-f. Maguer, R. Grover, and C. Ferrier-Pagès, “New insights into carbon acquisition and exchanges within the coral-dinoflagellate symbiosis under NH4+ and NO3 supply,” Proceedings of the Royal Society, vol. 282, Article ID 20150610.
  19. C. Pogoreutz, N. Rädecker, A. Cárdenas, A. Gärdes, C. R. Voolstra, and C. Wild, “Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching,” GCB Bioenergy, vol. 23, no. 9, pp. 3838–3848, 2017. View at Publisher · View at Google Scholar
  20. Z. Dubinsky and P. L. Jokiel, “Ratio of energy and nutrient fluxes regulate symbiosis between zooxanthellae and corals,” Pacific Science, vol. 48, no. 3, pp. 313–324, 1994. View at Google Scholar
  21. P. Tremblay, J. F. Maguer, R. Grover, and C. Ferrier-Pages, “Trophic dynamics of scleractinian corals: Stable isotope evidence,” Journal of Experimental Biology, vol. 218, no. 8, pp. 1223–1234, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Tremblay, R. Grover, J. F. Maguer, L. Legendre, and C. Ferrier-Pagès, “Autotrophic carbon budget in coral tissue: A new 13C-based model of photosynthate translocation,” Journal of Experimental Biology, vol. 215, no. 8, pp. 1384–1393, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. E. Erickson, S. Wakao, and K. K. Niyogi, “Light stress and photoprotection in Chlamydomonas reinhardtii,” The Plant Journal, vol. 82, no. 3, pp. 449–465, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. L. P. Suescún-Bolívar, G. M. I. Traverse, and P. E. Thomé, “Glycerol outflow in Symbiodinium under osmotic and nitrogen stress,” Marine Biology, vol. 163, no. 5, article no. 128, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Demmig-Adams, T. A. Burch, J. J. Stewart, E. L. Savage, and W. W. Adams, “Algal glycerol accumulation and release as a sink for photosynthetic electron transport,” Algal Research, vol. 21, pp. 161–168, 2017. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Grajales and E. Rodríguez, “Morphological revision of the genus Aiptasia and the family Aiptasiidae (Cnidaria, Actiniaria, etridioidea),” Zootaxa, vol. 3826, no. 1, pp. 55–100, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. R. G. Steen and L. Muscatine, “Low temperature evokes rapid exocytosis of symbiotic algae by a sea anemone,” Biological Bulletin, vol. 172, no. 2, pp. 246–263, 1987. View at Google Scholar
  28. L. Muscatine, D. Grossman, and J. Doino, “Release of symbiotic algae by tropical sea anemones and corals after cold shock,” Marine Ecology Progress Series, vol. 77, no. 2-3, pp. 233–243, 1991. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Bergmeyer, M. Gra, and M. Graβl, Methods of Enzymatic Analysis, vol. VI, 1988.
  30. J. Bergmeyer and M. Graßl, vol. 3 of Enzymes, VCH, Weinheim, Germany, 1987.
  31. W. K. Fitt and R. L. Pardy, “Effects of starvation, and light and dark on the energy metabolism of symbiotic and aposymbiotic sea anemones, Anthopleura elegantissima,” Marine Biology, vol. 61, no. 2-3, pp. 199–205, 1981. View at Publisher · View at Google Scholar · View at Scopus
  32. C. A. Oakley, M. F. Ameismeier, L. Peng, V. M. Weis, A. R. Grossman, and S. K. Davy, “Symbiosis induces widespread changes in the proteome of the model cnidarian Aiptasia,” Cellular Microbiology, vol. 18, no. 7, pp. 1009–1023, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. T. A. Garrett, J. L. Schmeitzel, J. A. Klein, J. J. Hwang, and J. A. Schwarz, “Comparative Lipid Profiling of the Cnidarian Aiptasia pallida and Its Dinoflagellate Symbiont,” PLoS ONE, vol. 8, no. 3, Article ID e57975, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. J.-J. Park, H. Wang, M. Gargouri et al., “The response of Chlamydomonas reinhardtii to nitrogen deprivation: A systems biology analysis,” The Plant Journal, vol. 81, no. 4, pp. 611–624, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Tremblay, R. Grover, J. F. Maguer, M. Hoogenboom, and C. Ferrier-Pagès, “Carbon translocation from symbiont to host depends on irradiance and food availability in the tropical coral Stylophora pistillata,” Coral Reefs, vol. 33, no. 1, pp. 1–13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. K. E. Hillyer, D. A. Dias, A. Lutz, U. Roessner, and S. K. Davy, “Mapping carbon fate during bleaching in a model cnidarian symbiosis: the application of 13C metabolomics,” New Phytologist, vol. 214, no. 4, pp. 1551–1562, 2017. View at Publisher · View at Google Scholar · View at Scopus
  37. S. R. Dunn, M. C. Thomas, G. W. Nette, and S. G. Dove, “A Lipidomic Approach to Understanding Free Fatty Acid Lipogenesis Derived from Dissolved Inorganic Carbon within Cnidarian-Dinoflagellate Symbiosis,” PLoS ONE, vol. 7, no. 10, Article ID e46801, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. A. B. Imbs and I. M. Yakovleva, “Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: An experimental approach,” Coral Reefs, vol. 31, no. 1, pp. 41–53, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Bachar, Y. Achituv, Z. Pasternak, and Z. Dubinsky, “Autotrophy versus heterotrophy: The origin of carbon determines its fate in a symbiotic sea anemone,” Journal of Experimental Marine Biology and Ecology, vol. 349, no. 2, pp. 295–298, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. K. E. Hillyer, S. Tumanov, S. Villas-Bôas, and S. K. Davy, “Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis,” Journal of Experimental Biology, vol. 219, no. 4, pp. 516–527, 2016. View at Publisher · View at Google Scholar · View at Scopus
  41. A. G. Grottoli, M. E. Warner, S. J. Levas et al., “The cumulative impact of annual coral bleaching can turn some coral species winners into losers,” GCB Bioenergy, vol. 20, no. 12, pp. 3823–3833, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. A. G. Grottoli and L. J. Rodrigues, “Bleached Porites compressa and Montipora capitata corals catabolize δ13C-enriched lipids,” Coral Reefs, vol. 30, no. 3, pp. 687–692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. A. B. Imbs, I. M. Yakovleva, T. N. Dautova, L. H. Bui, and P. Jones, “Diversity of fatty acid composition of symbiotic dinoflagellates in corals: Evidence for the transfer of host PUFAs to the symbionts,” Phytochemistry, vol. 101, pp. 76–82, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. E. M. Lehnert, M. E. Mouchka, M. S. Burriesci, N. D. Gallo, J. A. Schwarz, and J. R. Pringle, “Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians,” G3: Genes, Genomes, Genetics, vol. 4, no. 2, pp. 277–295, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. L. F. Whitehead and A. E. Douglas, “Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host,” Journal of Experimental Biology, vol. 206, no. 18, pp. 3149–3157, 2003. View at Publisher · View at Google Scholar · View at Scopus
  46. G. E. Fogg, Photosynthesis, Hodder and Stoughton, London, UK, 2nd edition, 1972.
  47. M. Pernice, A. Meibom, A. Van Den Heuvel et al., “A single-cell view of ammonium assimilation in coral-dinoflagellate symbiosis,” The ISME Journal, vol. 6, no. 7, pp. 1314–1324, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Tanaka, A. G. Grottoli, Y. Matsui, A. Suzuki, and K. Sakai, “Partitioning of nitrogen sources to algal endosymbionts of corals with long-term 15N-labelling and a mixing model,” Ecological Modelling, vol. 309-310, pp. 163–169, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Houlbrèque and C. Ferrier-Pagès, “Heterotrophy in tropical scleractinian corals,” Biological Reviews, vol. 84, no. 1, pp. 1–17, 2009. View at Publisher · View at Google Scholar · View at Scopus