The magnesium inhibition and arrested phagosome hypotheses: New perspectives on the evolution and ecology of Symbiodinium symbioses

Biological Reviews

Volumn 87, Issue 4, 2012, Pages 804-821

  Malcolm, Hill ^a   April, Hill ^a  

^a UNIVERSITY OF RICHMOND   (United States)

Author keywords

Metals; Paleooceans; Phagosomes; Photosynthesis; Sponges; Symbiodinium; Symbiosis

Indexed keywords

CALCIUM; MAGNESIUM;

ANIMAL; ANTHOZOA; ARTICLE; DINOFLAGELLATE; EVOLUTION; METABOLISM; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; ANTHOZOA; BIOLOGICAL EVOLUTION; CALCIUM; DINOFLAGELLIDA; MAGNESIUM; SYMBIOSIS;

ANTHOZOA; SYMBIODINIUM;

EID: 84867140106     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/j.1469-185X.2012.00223.x     Document Type: Article

References (269)

1. Adam, M. S. & Issa, A. A. (2000). Effect of manganese and calcium deficiency on the growth and oxygen exchange of Scenedesmus intermedius cultured for successive generations. Folia Microbiologica 45, 353-358.
2. Al-Horani, F. A., Al-Moghrabi, S. M. & de Beer, D. (2003). The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Marine Biology 142, 419-426.
3. Al-Horani, F. A., Tambutte, E. & Allemand, D. (2007). Dark calcification and the daily rhythm of calcification in the scleractinian coral, Galaxea fascicularis. Coral Reefs 26, 531-538.
4. Amin, S. A., Green, D. H., Hart, M. C., Kuepper, F. C., Sunda, W. G. & Carrano, C. J. (2009). Photolysis of iron-siderophore chelates promotes bacterial-algal mutualism. Proceedings of the National Academy of Sciences 106, 17071-17076.
5. Andras, J. P., Kirk, N. L. & Harvell, C. D. (2011). Range-wide population genetic structure of Symbiodinium associated with the Caribbean Sea fan coral, Gorgonia ventalina. Molecular Ecology 20, 2525-2542.
6. Baghdasarian, G. & Muscatine, L. (2000). Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biological Bulletin 199, 278-286.
7. Baker, A. C. (2002). Ecology - Is coral bleaching really adaptive? Reply. Nature 415, 602-602.
8. Baker, A. C. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology Evolution and Systematics 34, 661-689.
9. Baker, A. C. & Romanski, A. M. (2007). Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: comment on Goulet (2006). Marine Ecology: Progress Series 335, 237-242.
10. Barbeitos, M. S., Romano, S. L. & Lasker, H. R. (2010). Repeated loss of coloniality and symbiosis in scleractinian corals. Proceedings of the National Academy of Sciences 107, 11877-11882.
11. Bautista-Guerrero, E., Carballo, J. L., Cruz-Barraza, J. A. & Nava, H. H. (2006). New coral reef boring sponges (Hadromerida : Clionaidae) from the Mexican Pacific Ocean. Journal of the Marine Biological Association of the United Kingdom 86, 963-970.
12. de Baar, H. J. W., Boyd, P. W., Coale, K. H., Landry, M. R., Tsuda, A., Assmy, P., Bakker, D. C. E., Bozec, Y., Barber, R. T., Brzezinski, M. A., Buesseler, K. O., Boye, M., Croot, P. L., Gervais, F., Gorbunov, M. Y., Harrison, P. J., Hiscock, W. T., Laan, P., Lancelot, C., Law, C. S., Levasseur, M., Marchetti, A., Millero, F. J., Nishioka, J., Nojiri, Y., van Oijen, T., Riebesell, U., Rijkenberg, M. J. A., Saito, H., Takeda, S., Timmermans, K. R., Veldhuis, M. J. W., Waite, A. M. & Wong, C. S. (2005). Synthesis of iron fertilization experiments: from the iron age in the age of enlightenment. Journal of Geophysical Research: Oceans 110, C09S16.
13. Behrenfeld, M. J., Bale, A. J., Kolber, Z. S., Aiken, J. & Falkowski, P. G. (1996). Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383, 508-511.
14. Belda-Baillie, C. A., Baillie, B. K. & Maruyama, T. (2002). Specificity of a model cnidarian-dinoflagellate symbiosis. Biological Bulletin 202, 74-85.
15. Bertucci, A., Tambutte, E., Tambutte, S., Allemand, D. & Zoccola, D. (2010). Symbiosis-dependent gene expression in coral-dinoflagellate association: cloning and characterization of a P-type H+-ATPase gene. Proceedings of the Royal Society B: Biological Sciences 277, 87-95.
16. Böhm, F., Joachimski, M. M., Dullo, W-C., Eisenhauer, A., Lehnert, H., Reitner, J. & Wörheide, G. (2000). Oxygen isotope fractionation in marine aragonite of coralline sponges. Geochimica et Cosmochimica Acta 64, 1695-1703.
17. Bonny, O., Rubin, A., Huang, C., Frawley, W. H., Pak, C. Y. C. & Moe, O. W. (2008). Mechanism of urinary calcium regulation by urinary magnesium and pH. Journal of the American Society of Nephrology 19, 1530-1537.
18. Borowitzka, M. (1982). Morphological and cytological aspects of algal calcification. International Review of Cytology: A Survey of Cell Biology 74, 127-162.
19. Boschma, H. (1925). On the feeding reactions and digestion in the coral polyp Astrangia danae, with notes on its symbionts with zooxanthellae. Biological Bulletin 49, 407-439.
20. Boulais, J., Trost, M., Landry, C. R., Dieckmann, R., Levy, E. D., Soldati, T., Michnick, S. W., Thibault, P. & Desjardins, M. (2010). Molecular characterization of the evolution of phagosomes. Molecular Systems Biology 6, 423.
21. Bronstein, J. L. (2001). The exploitation of mutualisms. Ecological Letters 4, 277-287.
22. Bruland, K. W., Orians, K. J. & Cowen, J. P. (1994). Reactive trace-metals in the stratified central North Pacific. Geochimica et Cosmochimica Acta 58, 3171-3182.
23. Buddemeier, R. W. & Fautin, D. G. (1993). Coral bleaching as an adaptive mechanism-a testable hypothesis. Bioscience 43, 320-326.
24. Burdige, D. J., Zimmerman, R. C. & Hu, X. (2008). Rates of carbonate dissolution in permeable sediments estimated from pore-water profiles: the role of sea grasses. Limnology and Oceanography 53, 549-565.
25. 2+-antagonist phenothiazine drugs. Plant Physiology 71, 712-715.
26. Cairns, S. D. (2007). Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bulletin of Marine Science 81, 311-322.
27. Carafoli, E. (1987). Intracellular calcium homeostasis. Annual Review of Biochemistry 56, 395-433.
28. Carlos, A. A., Baillie, B. K., Kawachi, M. & Maruyama, T. (1999). Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. Journal of Phycology 35, 1054-1062.
29. Cavalier-Smith, T. (1992). The number of symbiotic origins of organelles. Biosystems 28, 91-106.
30. Chalker, B. E. (1976). Calcium-transport during skeletogenesis in hermatypic corals. Comparative Biochemistry and Physiology A-Physiology 54, 455-459.
31. Chapin, T. P., Johnson, K. S. & Coale, K. H. (1991). Rapid determination of manganese in seawater by flow-injection analysis with chemiluminescence detection. Analytica Chimica Acta 249, 469-478.
32. Chen, M., Cheng, Y., Hong, M. & Fang, L. (2004). Molecular cloning of Rab5 (ApRab5) in Aiptasia pulchella and its retention in phagosomes harboring live zooxanthellae. Biochemical and Biophysical Research Communications 324, 1024-1033.
33. Chen, M., Cheng, Y., Sung, P., Kuo, C. & Fang, L. (2003). Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochemical and Biophysical Research Communications 308, 586-595.
34. Chen, Z., Harb, O. S. & Roos, D. S. (2008). In silico identification of specialized secretory-organelle proteins in apicomplexan parasites and in vivo validation in Toxoplasma gondii. PLoS ONE 3, e3611.
35. Coale, K. H. (1991). Effects of iron, manganese, copper, and zinc enrichments on productivity and biomass in the subarctic Pacific. Limnology and Oceanography 36, 1851-1864.
36. Coats, D. W. (1999). Parasitic life styles of marine dinoflagellates. Journal of Eukaryotic Microbiology 46, 402-409.
37. Coffroth, M. A., Lewis, C. F., Santos, S. R. & Weaver, J. L. (2006). Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Current Biology 16, 985-987.
38. Coffroth, M. & Santos, S. (2005). Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156, 19-34.
39. Coffroth, M., Santos, S. & Goulet, T. (2001). Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Marine Ecology-Progress Series 222, 85-96.
40. Colley, N. J. & Trench, R. K. (1983). Selectivity in phagocytosis and persistence of symbiotic algae by the scyphistoma stage of the jellyfish Cassiopeia-Xamachana. Proceedings of the Royal Society B 219, 61-82.
41. Colley, N. J. & Trench, R. K. (1985). Cellular events in the reestablishment of a symbiosis between a marine dinoflagellate and a coelenterate. Cell and Tissue Research 239, 93-103.
42. Correa, A. M. S., McDonald, M. D. & Baker, A. C. (2009). Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Marine Biology 156, 2403-2412.
43. Culotta, V. C., Yang, M. & Hall, M. D. (2005). Manganese transport and trafficking: lessons learned from Saccharomyces cerevisiae. Eukaryotic Cell 4, 1159-1165.
44. Davy, S. K., Lucas, I. A. N. & Turner, J. R. (1997). Uptake and persistence of homologous and heterologous zooxanthellae in the temperate sea anemone Cereus pedunculatus (Pennant). Biological Bulletin 192, 208-216.
45. Delwiche, C. F. (2007). The origin and evolution of dinoflagellates. In Evolution of Primary Producers in the sea (eds P. G. Falkowski and A. H. Knoll), pp. 191-205. Elsever, New York.
46. Dimond, J. & Carrington, E. (2008). Symbiosis regulation in a facultatively symbiotic temperate coral: zooxanthellae division and expulsion. Coral Reefs 27, 601-604.
47. Docampo, R., Ulrich, P. & Moreno, S. N. J. (2010). Evolution of acidocalcisomes and their role in polyphosphate storage and osmoregulation in eukaryotic microbes. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 775-784.
48. Domotor, S. L. & D'Elia, C. F. (1986). Cell-size distributions of zooxanthellae in culture and symbiosis. Biological Bulletin 170, 519-525.
49. Douglas, A. E. (2010). The Symbiotic Habit Princeton University Press, Princeton.
50. Downs, C. A., Kramarsky-Winter, E., Martinez, J., Kushmaro, A., Woodley, C. M., Loya, Y. & Ostrander, G. K. (2009). Symbiophagy as a cellular mechanism for coral bleaching. Autophagy 5, 211-216.
51. Dubilier, N., Bergin, C. & Lott, C. (2008). Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nature Reviews Microbiology 6, 725-740.
52. Dunn, S. R. & Weis, V. M. (2009). Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environmental Microbiology 11, 268-276.
53. Edmunds, P. J. & Gates, R. D. (2003). Has coral bleaching delayed our understanding of fundamental aspects of coral-dinoflagellate symbioses? Bioscience 53, 976-980.
54. Enyedi, A., Sarkadi, B. & Gardos, G. (1982). On the substrate-specificity of the red-cell calcium-pump. Biochimica et Biophysica Acta 687, 109-112.
55. Eva, A. N. (1980). Pre-Miocene seagrass communities in the Caribbean. Palaeontology 23, 231-236.
56. Fadlallah, Y. H. (1983). Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2, 129-150.
57. Fagoonee, I., Wilson, H. B., Hassell, M. P. & Turner, J. R. (1999). The dynamics of zooxanthellae populations: a long-term study in the field. Science 283, 843-845.
58. Falkowski, P. G., Dubinsky, Z., Muscatine, L. & McCloskey, L. (1993). Population control in symbiotic corals. BioScience 43, 606-611.
59. Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A., Raven, J. A., Schofeld, O. & Taylor, F. J. R. (2004). The evolution of modern eukaryotic phytoplankton. Science 305, 354-360.
60. Fang, L. S., Chen, Y. W. J. & Chen, C. S. (1989). Why does the white tip of stony coral grow so fast without zooxanthellae. Marine Biology 103, 359-363.
61. Fankboner, P. V. (1971). Intracellular digestion of symbiontic zooxanthellae by host amoebocytes in giant clams (Bivalvia: Tridacnidae), with a note on the nutritional roles of the hypertrophied siphonal epidermis. Biological Bulletin 141, 222-234.
62. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. (2004). Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838.
63. Ferrier-Pages, C., Schoelzke, V., Jaubert, J., Muscatine, L. & Hoegh-Guldberg, O. (2001). Response of a scleractinian coral, Stylophora pistillata, to iron and nitrate enrichment. Journal of Experimental Marine Biology and Ecology 259, 249-261.
64. Finney, J. C., Pettay, D. T., Sampayo, E. M., Warner, M. E., Oxenford, H. A. & LaJeunesse, T. C. (2010). The relative significance of host-habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microbial Ecology 60, 250-263.
65. Fitt, W. K. (1985a). Chemosensory responses of the symbiotic dinoflagellate Symbiodinium microadriaticum (Dinophyceae). Journal of Phycology 21, 62-67.
66. Fitt, W. K. (1985b). Effect of different strains of the zooxanthella Symbiodinium microadriaticum on growth and survival of their coelenterate and molluscan hosts. Proceedings of the 5th International Coral Reef Congress, Tahiti, Volume 6, pp. 131-136.
67. Fitt, W. K. (2000). Cellular growth of host and symbiont in a cnidarian-zooxanthellar symbiosis. Biological Bulletin 198, 110-120.
68. Fitt, W. K., McFarland, F. K., Warner, M. E. & Chilcoat, G. C. (2000). Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnology Oceanography 45, 677-685.
69. Fitt, W. K. & Trench, R. K. (1983a). Endocytosis of the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal by endodermal cells of the scyphistomae of Cassiopeia-Xamachana and resistance of the algae to host digestion. Journal of Cell Science 64, 195-212.
70. Fitt, W. K. & Trench, R. K. (1983b). The relation of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New Phytologist 94, 421-432.
71. Flatman, P. W. (1984). Magnesium transport across cell-membranes. Journal of Membrane Biology 80, 1-14.
72. Franklin, D. J., Hoegh-Guldberg, O., Jones, R. J. & Berges, J. A. (2004). Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Marine Ecology Progress Series 272, 117-130.
73. Fricke, H. W., Vareschi, E. & Schlichter, D. (1987). Photoecology of the coral Leptoseris fragilis in the Red Sea Twilight Zone (an experimental study by submersible). Oecologia 73, 371-381.
74. Fry, C. & Hall, S. (1990). The role of magnesium in the regulation of muscle function. Metal Ions in Biological Systems 26, 463-488.
75. Garcia-Cuetos, L., Pochon, X. & Pawlowski, J. (2005). Molecular evidence for host-symbiont specificity in soritid Foraminifera. Protist 156, 399-412.
76. Garrison, T. (2007). Oceanography: An Invitation to Marine Science Sixth Edition. Thompson Brooks/Cole, Belmont, CA.
77. Garson, M. J., Flowers, A. E., Webb, R. I., Charan, R. D. & McCaffrey, E. J. (1998). A sponge/dinoflagellate association in the haplosclerid sponge Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation. Cell and Tissue Research 293, 365-373.
78. Gast, R. J. & Caron, D. A. (1996). Molecular phylogeny of symbiotic dinoflagellates from plankton foraminifera and radiolaria. Molecular Biology and Evolution 13, 1192-1197.
79. Ghirelli, F. & Leckner, B. (2004). Transport equation for the local residence time of a fluid. Chemical Engineering Science 59, 513-523.
80. Goulet, T. L. (2006). Most corals may not change their symbionts. Marine Ecology: Progress Series 321, 1-7.
81. Goulet, T. L. (2007). Most scleractinian corals and octocorals host a single symbiotic zooxanthella clade. Marine Ecology: Progress Series 335, 243-248.
82. Granados, C., Camargo, C., Zea, S. & Sanchez, J. A. (2008). Phylogenetic relationships among zooxanthellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpected lineage in the Caribbean. Molecular Phylogenetics and Evolution 49, 554-560.
83. Grant, A. J., Rémond, M., Starke-Peterkovic, T. & Hinde, R. (2006). A cell signal from the coral Plesiastrea versipora reduces starch synthesis in its symbiotic alga, Symbiodinium sp. Comparative Biochemistry and Physiology, Part A, 144, 458-463.
84. Grant, A. J., Starke-Peterkovic, T., Withers, K. J. T. & Hinde, R. (2004). Aposymbiotic Plesiastrea versipora continues to produce cell-signalling molecules that regulate the carbon metabolism of symbiotic algae. Comparative Biochemistry and Physiology, Part A 138, 253-259.
85. Griffith, E. M., Paytan, A., Caldeira, K., Bullen, T. D. & Thomas, E. (2008). A dynamic marine calcium cycle during the past 28 million years. Science 322, 1671-1674.
86. Hackett, J. D., Anderson, D. M., Erdner, D. L. & Bhattacharya, D. (2004). Dinoflagellates: a remarkable evolutionary experiment. American Journal of Botany 91, 1523-1534.
87. Hakala, M., Tuominen, I., Keranen, M., Tyystjarvi, T. & Tyystjarvi, E. (2005). Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochimica et Biophysica Acta: Bioenergetics 1706, 68-80.
88. Hardie, L. A. (1996). Secular variation in seawater chemistry: an explanation for the coupled secular variation in the mineralogies of marine limestones and potash evaporites over the past 600 my. Geology 24, 279-283.
89. Hatch, W. (1980). The implication of carbonic-anhydrase in the physiological mechanism of penetration of carbonate substrata by the marine burrowing sponge Cliona celata (Demospongiae). Biological Bulletin 159, 135-147.
90. Hill, M. S. (1996). Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Marine Biology 125, 649-654.
91. Hill, M., Allenby, A., Ramsby, B., Schönberg, C. & Hill, A. (2011). Symbiodinium diversity among host clionaid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Molecular Phylogenetics and Evolution 59, 81-88.
92. Hill, R., Ulstrup, K. E. & Ralph, P. J. (2009). Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. Bulletin of Marine Science 85, 223-244.
93. Hill, M. S. & Wilcox, T. M. (1998). Unusual mode of symbiont acquisition after bleaching in the tropical sponge Anthosigmella varians: acquisition of different zooxanthellae strains? Symbiosis 25, 279-289.
94. Hille, B. (2001). Ion Channels of Excitable Membranes Third Edition. Sinauer Associates, Sunderland, Massachusetts.
95. 2+ current in Paramecium. Proceedings of the National Academy of Sciences 99, 15717-15722.
96. Hirose, M. & Hidaka, M. (2006). Early development of zooxanthella-containing eggs of the corals Porites cylindrica and Montipora digitata: the endodermal localization of zooxanthellae. Zoological Science 23, 873-881.
97. Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50, 839-866.
98. Hoegh-Guldberg, O. & Bruno, J. F. (2010). The impact of climate change on the world's marine ecosystems. Science 328, 1523-1528.
99. Hoegh-Guldberg, O., Jones, R. J., Ward, S. & Loh, W. K. (2002). Ecology-is coral bleaching really adaptive? Nature 415, 601-602.
100. Hong, M., Huang, Y., Song, P., Lin, W., Fang, L. & Chen, M. (2009). Cloning and characterization of ApRab4, a recycling Rab protein of Aiptasia pulchella, and its implication in the symbiosome biogenesis. Marine Biotechnology 11, 771-785.
101. Horibe, Y., Endo, K. & Tsubota, H. (1974). Calcium in the South Pacific, and its correlation with carbonate alkalinity. Earth and Planetary Science Letters 23, 136-140.
102. Huang, H. J., Wang, L. H., Chen, W. N. U., Fang, L. S. & Chen, C. S. (2008). Developmentally regulated localization of endosymbiotic dinoflagellates in different tissue layers of coral larvae. Coral Reefs 27, 365-372.
103. Hunt, D. E., David, L. A., Gevers, D., Preheim, S. P., Alm, E. J. & Polz, M. F. (2008). Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320, 1081-1085.
104. Iglesias-Prieto, R., Beltran, V. H., LaJeunesse, T. C., Reyes-Bonilla, H. & Thome, P. E. (2004). Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Philosophical Transactions of the Royal Society B: Biological Sciences 271, 1757-1763.
105. Iseri, L. T. & French, J. H. (1984). Magnesium-Nature's physiologic calcium blocker. American Heart Journal 108, 188-193.
106. Johnson, K. S., Gordon, R. M. & Coale, K. H. (1997). What controls dissolved iron concentrations in the world ocean? Marine Chemistry 57, 137-161.
107. Jones, R. J. & Yellowlees, D. (1997). Regulation and control of intracellular algae (= zooxanthellae) in hard corals. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 352, 457-468.
108. Kanady, J. S., Tsui, E. Y., Day, M. W. & Agapie, T. (2011). A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II. Science 333, 733-736.
109. Katz, M., Finkel, Z., Grzebyk, D., Knoll, A. & Falkowski, P. (2004). Evolutionary trajectories and biogeochemical impacts of marine eukaryotic phytoplankton. Annual Review of Ecology Evolution and Systematics 35, 523-556.
110. Kawaguchi, S. (1944). On the physiology of reef corals. VII. The zooxanthella of the reef corals is Gymnodinium sp. Dinoflagellata its culture in vitro. Palao Tropical Biological Station Studies 2, 675-679.
111. Kempf, S. (1984). Symbiosis between the zooxanthella Symbiodinium (= Gymnodinium) microadriaticum (Freudenthal) and 4 species of nudibranchs. Biological Bulletin 166, 110-126.
112. Kessler, H., Herm-Götz, A., Hegge, S., Rauch, M., Soldati-Favre, D., Frischknecht, F. & Meissner, M. (2008). Microneme protein 8-a new essential invasion factor in Toxoplasma gondii. Journal of Cell Science 121, 947-956.
113. Kiers, E. T., Palmer, T. M., Ives, A. R., Bruno, J. F. & Bronstein, J. L. (2010). Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13, 1459-1474.
114. Kinzie, R. & Chee, G. (1979). Effect of different zooxanthellae on the growth of experimentally re-infected hosts. Biological Bulletin 156, 315-327.
115. Kinzie, R. A., Takayama, M., Santos, S. R. & Coffroth, M. A. (2001). The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biological Bulletin 200, 51-58.
116. Kodama, Y. & Fujishima, M. (2010). Secondary symbiosis between Paramecium and Chlorella cells. International Review of Cell and Molecular Biology 279, 33-77.
117. Koike, K., Jimbo, M., Sakai, R., Kaeriyama, M., Muramoto, K., Ogata, T., Maruyama, T. & Kamiya, H. (2004). Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biological Bulletin 207, 80-86.
118. Kuo, J., Liang, Z. & Lin, C. (2010). Suppression subtractive hybridization identifies genes correlated to symbiotic and aposymbiotic sea anemone associated with dinoflagellate. Journal of Experimental Marine Biology and Ecology 388, 11-19.
119. Kvennefors, E. C. E., Leggat, W., Hoegh-Guldberg, O., Degnan, B. M. & Barnes, A. C. (2008). An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Developmental and Comparative Immunology 32, 1582-1592.
120. LaJeunesse, T. C. (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. Journal of Phycology 37, 866-880.
121. LaJeunesse, T. C. (2002). Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141, 387-400.
122. LaJeunesse, T. C. (2005). "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Molecular Biology and Evolution 22, 570-581.
123. LaJeunesse, T., Lee, S., Bush, S. & Bruno, J. (2005). Persistence of non-Caribbean algal symbionts in Indo-Pacific mushroom corals released to Jamaica 35 years ago. Coral Reefs 24, 157-159.
124. LaJeunesse, T. C., Smith, R., Walther, M., Pinzón, J., Pettay, D. T., McGinley, M., Aschaffenburg, M., Medina-Rosas, P., Cupul-Magana, A., Pérez, A. L., Reyes-Bonilla, H. & Warner, M. E. (2010). Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proceedings of the Royal Society B 277, 2925-2934
125. Langer, M. R. & Lipps, J. H. (1995). Phylogenetic incongruence between dinoflagellate endosymbionts (Symbiodinium) and their host foraminifera (Sorites): small-subunit ribosomal RNA gene sequence evidence. Marine Micropaleontology 26, 179-186.
126. Leander, B. S. & Keeling, P. J. (2003). Morphostasis in alveolate evolution. Trends in Ecology and Evolution 18, 395-402.
127. Leletkin, V. A. (2000). Trophic status and population density of zooxanthellae in hermatypic corals. Russian 26, 231-240.
128. Lesser, M. P. (1996). Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnology and Oceanography 41, 271-283.
129. Levy, O., Kaniewska, P., Alon, S., Eisenberg, E., Karako-Lampert, S., Bay, L. K., Reef, R., Rodriguez-Lanetty, M., Miller, D. J. & Hoegh-Guldberg, O. (2011). Complex diel cycles of gene expression in coral-algal symbiosis. Science 331, 175-175.
130. Lewis, C. L. & Coffroth, M. A. (2004). The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304, 1490-1492.
131. Lindner, A., Cairns, S. D. & Cunningham, C. W. (2008). From offshore to onshore: multiple origins of shallow-water corals from deep-sea ancestors. PLoS ONE 3, e2429.
132. Little, A., van Oppen, M. & Willis, B. (2004). Flexibility in algal endosymbioses shapes growth in reef corals. Science 304, 1492-1494.
133. Littman, R. A., van Oppen, M. J. H. & Willis, B. L. (2008). Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). Journal of Experimental Marine Biology and Ecology 364, 48-53.
134. Lowenstein, T., Hardie, L., Timofeeff, M. & Demicco, R. (2003). Secular variation in seawater chemistry and the origin of calcium chloride basinal brines. Geology 31, 857-860.
135. Lowenstein, T., Timofeeff, M., Brennan, S., Hardie, L. & Demicco, R. (2001). Oscillations in Phanerozoic seawater chemistry: evidence from fluid inclusions. Science 294, 1086-1088.
136. Maguire, M. & Cowan, J. (2002). Magnesium chemistry and biochemistry. Biometals 15, 203-210.
137. Maldonado, M., Cortadellas, N., Trillas, M. I. & Rutzler, K. (2005). Endosymbiotic yeast maternally transmitted in a marine sponge. Biological Bulletin 209, 94-106.
138. Mariani, S., Uriz, M-J. & Turon, X. (2000). Larval bloom of the oviparous songe Cliona viridis: coupling of larval abundance and adult distribution. Marine Biology 137, 783-790.
139. Marlow, H. Q. & Martindale, M. Q. (2007). Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evolution & Development 9, 355-367.
140. Marshall, A. T. (1996). Calcification in hermatypic and ahermatypic corals. Science 271, 637-639.
141. Marshall, A. T. & Clode, P. L. (2002). Effect of increased calcium concentration in sea water on calcification and photosynthesis in the scleractinian coral Galaxea fascicularis. Journal of Experimental Biology 205, 2107-2113.
142. Marshall, A. T., Clode, P. L., Russell, R., Prince, K. & Stern, R. (2007). Electron and ion microprobe analysis of calcium distribution and transport in coral tissues. Journal of Experimental Biology 210, 2453-2463.
143. Martens, C., Vandepoele, K. & van de Peer, Y. (2008). Whole-genome analysis reveals molecular innovations and evolutionary transitions in chromalveolate species. Proceedings of the National Academy of Sciences 105, 3427-3432.
144. Martin, J. H., Gordon, R. M. & Fitzwater, S. E. (1990). Iron in Antarctic waters. Nature 345, 156-158.
145. Maruyama, T. & Heslinga, G. (1997). Fecal discharge of zooxanthellae in the giant clam Tridacna derasa, with reference to their in situ growth rate. Marine Biology 127, 473-477.
146. McCloskey, L. R., Cove, T. G. & Verde, E. A. (1996). Symbiont expulsion from the anemone Anthopleura elegantissima (Brandt) (Cnidaria; Anthozoa). Journal of Experimental Marine Biology and Ecology 195, 173-186.
147. McConnaughey, T. A. & Falk, R. H. (1991). Calcium-proton exchange during algal calcification. Biological Bulletin 180, 185-195.
148. McConnaughey, T. A. & Whelan, J. F. (1997). Calcification generates protons for nutrient and bicarbonate uptake. Earth: Science Reviews 42, 95-117.
149. McFall-Ngai, M. (2008). Are biologists in 'future shock'? Symbiosis integrates biology across domains. Nature Reviews Microbiology 6, 789-792.
150. Miller, R. S. (1967). Pattern and process in competition. In Advances in Ecological Research (ed. J. B. Cragg), pp. 1-74. Academic Press, San Diego.
151. Mitchelmore, C., Schwarz, J. & Weis, V. (2002). Development of symbiosis-specific genes as biomarkers for the early detection of cnidarian-algal symbiosis breakdown. Marine Environmental Research 54, 345-349.
152. Moore, C. M., Mills, M. M., Milne, A., Langlois, R., Achterberg, E. P., Lochte, K., Geider, R. J. & La Roche, J. (2006). Iron limits primary productivity during spring bloom development in the central North Atlantic. Global Change Biology 12, 626-634.
153. Moreno, S. N. J. & Docampo, R. (2009). The role of acidocalcisomes in parasitic protists. Journal of Eukaryotic Microbiology 56, 208-213.
154. Muller, E. B., Kooijman, S. A. L. M., Edmunds, P. J., Doyle, F. J. & Nisbet, R. M. (2009). Dynamic energy budgets in syntrophic symbiotic relationships between heterotrophic hosts and photoautotrophic symbionts. Journal of Theoretical Biology 259, 44-57.
155. Muscatine, L. (1967). Glycerol excretion by symbiotic algae from corals and Tridacna, and its control by the host. Science 156, 516-519.
156. Muscatine, L. & Porter, J. W. (1977). Reef corals-mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454-460.
157. Muscatine, L. & Weis, V. M. (1992). Productivity of zooxanthellae and biogeochemical cycles. In Primary Productivity and Biogeochemical Cycles in the Sea (eds P. G. Falkowski and A. D. Woodhead), pp. 257-268. Plenum Press, New York.
158. Nachshen, D. & Blaustein, M. (1982). Influx of calcium, strontium, and barium in pre-synaptic nerve-endings. Journal of General Physiology 79, 1065-1087.
159. Nava, H. & Carballo, J. L. (2008). Chemical and mechanical bioerosion of boring sponges from Mexican Pacific coral reefs. Journal of Experimental Biology 211, 2827-2831.
160. Neumann, A. C. (1966). Observations on coastal erosion in Bermuda and measurements of the boring rate of the sponge, Cliona lampa. Limnology and Oceanography 11, 92-108.
161. Norton, J., Shepherd, M., Long, H. & Fitt, W. (1992). The zooxanthellal tubular system in the giant clam. Biological Bulletin 183, 503-506.
162. van Oppen, M. (2004). Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Marine Biology 144, 1-7.
163. van Oppen, M., Mieog, J., Sanchez, C. & Fabricius, K. (2005). Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Molecular Ecology 14, 2403-2417.
164. Paasche, E. (1968). Biology and physiology of coccolithophorids. 22, 77-86.
165. Peng, S., Wang, Y., Wang, L., Chen, W. U., Lu, C., Fang, L. & Chen, C. (2010). Proteomic analysis of symbiosome membranes in cnidaria-dinoflagellate endosymbiosis. Proteomics 10, 1002-1016.
166. Perez, S. & Weis, V. M. (2006). Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. Journal of Experimental Biology 209, 2804-10.
167. Pochon, X. & Gates, R. D. (2010). A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai'i. Molecular Phylogenetics and Evolution 56, 492-497.
168. Pochon, X., Montoya-Burgos, J., Stadelmann, B. & Pawlowski, J. (2006). Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Molecular Phylogenetics and Evolution 38, 20-30.
169. Pochon, X., Stat, M., Takabayashi, M., Chasqui, L., Chauka, L. J., Logan, D. D. K. & Gates, R. D. (2010). Comparison of endosymbiotic and free-living Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. Journal of Phycology 46, 53-65.
170. Polne-Fuller, M. (1991). A novel technique for preparation of axenic cultures of Symbiodinium (Pyrrophyta) through selective digestion by amoebae. Journal of Phycology 27, 552-554.
171. Pomponi, S. (1979). Ultrastructure of cells associated with excavation of calcium-carbonate substrates by boring sponges. Journal of the Marine Biological Association of the United Kingdom 59, 777-790.
172. Quigg, A., Finkel, Z. V., Irwin, A. J., Rosenthal, Y., Ho, T-Y., Reinfelder, J. R., Schofeld, O., Morel, F. M. M. & Falkowski, P. G. (2003). The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425, 291-294.
173. Ragni, M., Airs, R. L., Hennige, S. J., Suggett, D. J., Warner, M. E. & Geider, R. J. (2010). PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Marine Ecology: Progress Series 406, 57-70.
174. Rands, M., Loughman, B. & Douglas, A. (1993). The symbiotic interface in an alga invertebrate symbiosis. Proceedings of the Royal Society B 253, 161-165.
175. 2-evolving organisms. Photosynthesis Research 60, 111-149.
176. Read, D. J. (1991). Mycorrhizas in ecosystems. Experientia 47, 376-391.
177. Reed, K. C., Muller, E. M. & van Woesik, R. (2010). Coral immunology and resistance to disease. Diseases of Aquatic Organisms 90, 85-92.
178. Reynolds, W., Schwarz, J. & Weis, V. (2000). Symbiosis-enhanced gene expression in cnidarian-algal associations: cloning and characterization of a cDNA, sym32, encoding a possible cell adhesion protein. Comparative Biochemistry and Physiology A: Molecular and Integrative Physiology 126, 33-44.
179. Richards, S. A., Nisbet, R. M., Wilson, W. G. & Possingham, H. P. (2000). Grazers and diggers: exploitation competition and coexistence among foragers with different feeding strategies on a single resource. American Naturalist 155, 266-279.
180. Richardson, S. (2001). Endosymbiont change as a key innovation in the adaptive radiation of Soritida (Foraminifera). Paleobiology 27, 262-289.
181. Ries, J. (2006). Aragonitic algae in calcite seas: effect of seawater Mg/Ca ratio on algal sediment production. Journal of Sedimentary Research 76, 515-523.
182. Ries, J. B. (2010). Review: geological and experimental evidence for secular variation in seawater Mg/Ca (calcite-aragonite seas) and its effects on marine biological calcification. Biogeosciences 7, 2795-2849.
183. Ries, J. B., Stanley, S. M. & Hardie, L. A. (2006). Scleractinian corals produce calcite, and grow more slowly, in artificial Cretaceous seawater. Geology 34, 525-528.
184. Rillig, M. C. (2004). Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7, 740-754.
185. Robison, J. & Warner, M. (2006). Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). Journal of Phycology 42, 568-579.
186. Rodriguez-Lanetty, M., Wood-Charlson, E. M., Hollingsworth, L. L., Krupp, D. A. & Weis, V. M. (2006). Temporal and spatial infection dynamics indicate recognition events in the early hours of a dinoflagellate/coral symbiosis. Marine Biology 149, 713-719.
187. Romano, S. L. & Palumbi, S. R. (1996). Evolution of scleractinian corals inferred from molecular systematics. Science 271, 640-642.
188. Rosell, D. & Uriz, M. J. (1992). Do associated zooxanthellae and the nature of the substratum affect survival, attachment and growth of Cliona viridis (Porifera, Hadromerida)? An experimental approach. Marine Biology 114, 503-507.
189. Roth, K. E., Jeon, K. & Stacy, G. (1988). Homology in endosymbiotic systems: the term "Symbiosome". In Molecular Genetics of Plant-Microbe Interactions (eds R. Palacios and D. P. S. Verma), pp. 220-225. APS Press, St. Paul.
190. Rowan, R. (2004). Coral bleaching - thermal adaptation in reef coral symbionts. Nature 430, 742-742.
191. Rowan, R., Knowlton, N., Baker, A. & Jara, J. (1997). Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265-269.
192. Rowan, R. & Powers, D. (1991a). A molecular genetic classification of Zooxanthellae and the evolution of animal-algal symbioses. Science 251, 1348-1351.
193. Rowan, R. & Powers, D. (1991b). Molecular genetic identification of symbiotic dinoflagellates (Zooxanthellae). Marine Ecology: Progress Series 71, 65-73.
194. Rowan, R. & Powers, D. (1992). Ribosomal-RNA sequences and the diversity of symbiotic dinoflagellates (Zooxanthellae). Proceedings of the National Academy of Sciences 89, 3639-3643.
195. Rudman, W. (1981). The anatomy and biology of alcyonarian-feeding aeolid opisthobranch mollusks and their development of symbiosis with zooxanthellae. Zoological Journal of the Linnean Society 72, 219-262.
196. Rutherford, A. W. & Faller, P. (2003). Photosystem II: evolutionary perspectives. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 358, 245-253.
197. Rützler, K. (1975). The role of burrowing sponges in bioerosion. Oecologia 19, 203-216.
198. Rützler, K. (1990). Associations between Caribbean sponges and photosynthetic organisms. In New Perspectives in Sponge Biology (ed. K. Rutzler), pp. 455-466. Smithsonian Institution Press, Washington, DC.
199. Sachs, J. L., Essenberg, C. J. & Turcotte, M. M. (2011). New paradigms for the evolution of beneficial infections. Trends in Ecology & Evolution 26, 202-209.
200. Sachs, J. L. & Wilcox, T. P. (2006). A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proceedings of the Royal Society B: Biological Sciences 273, 425-429.
201. Saenger, W., Jordan, P. & Krauss, N. (2002). The assembly of protein subunits and cofactors in photosystem. Current Opinion in Structural Biology 12, 244-254.
202. Salcedo, S. P. & Holden, D. W. (2005). Bacterial interactions with the eukaryotic secretory pathway. Current Opinion in Structural Biology 8, 92-98.
203. Saldarriaga, J. F., McEwan, M. L., Fast, N. M., Taylor, F. J. R. & Keeling, P. J. (2003). Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. International Journal of Systematic and Evolutionary Microbiology 53, 355-365.
204. de Salvo, M. K., Sunagawa, S., Fisher, P. L., Voolstra, C. R., Iglesias-Prieto, R. & Medina, M. (2010). Coral host transcriptomic states are correlated with Symbiodinium genotypes. Molecular ecology 19, 1174-1186.
205. Sampayo, E. M., Ridgway, T., Bongaerts, P. & Hoegh-Guldberg, O. (2008). Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of the National Academy of Sciences 105, 10444-10449.
206. Sandberg, P. A. (1983). An oscillating trend in phanerozoic non-skeletal carbonate mineralogy. Nature 305, 19-22.
207. Santos, S., Gutierrez-Rodriguez, C. & Coffroth, M. (2003). Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)-ribosomal DNA sequences. Marine Biotechnology 5, 130-140.
208. Sarà, M. & Liaci, L. (1964). Symbiotic associations between zooxanthellae and two marine sponges of the genus Cliona. Nature 203, 321.
209. Scalera-Liaci, L., Sciscioli, M., Lepore, E. & Gaino, E. (1999). Symbiotic zooxanthellae in Cinachyra tarentina, a non-boring demosponge. Endocytobiosis and Cell Research 13, 105-114.
210. Schönberg, C. H. L. (2008). A history of sponge erosion: from past myths and hypotheses to recent approaches. In Current Developments in Bioerosion (eds M. Wisshak and L. Tapanila), pp. 165-202. Springer, Berlin, Heidelberg.
211. Schönberg, C. H. L., de Beer, D. & Lawton, A. (2005). Oxygen microsensor studies on zooxanthellate clionaid sponges from the Costa Brava, Mediterranean Sea. Journal of Phycology 41, 774-779.
212. Schönberg, C. H. L. & Loh, W. K. W. (2005). Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis. Marine Ecology: Progress Series 299, 157-166.
213. Schönberg, C. H. L. & Suwa, R. (2007). Why bioeroding sponges may be better hosts for symbiotic dinoflagellates than many corals. In Porifera Research: Biodiversity, Innovation, and Sustainability. Proceedings of the 7th International Sponge Symposium, Buzios, Brazil (eds M. R. Cutodio, E. Hajdu, G. Lobo-Hajdu and G. Muricy), pp. 569-580. Museu Nacional, Rio de Janeiro.
214. Schönberg, C. H. L., Suwa, R., Hidaka, M. & Loh, W. K. W. (2008). Sponge and coral zooxanthellae in heat and light: preliminary results of photochemical efficiency monitored with pulse amplitude modulated fluorometry. Marine Ecology: An Evolutionary Perspective 29, 247-258.
215. Schwarz, J. A. (2008). Understanding the intracellular niche in cnidarian-Symbiodinium symbioses: parasites lead the way. Vie et Milieu: Life and Environment 58, 141-151.
216. Schwarz, J. & Weis, V. (2003). Localization of a symbiosis-related protein, sym32, in the Anthopleura elegantissima-Symbiodinium muscatinei association. Biological Bulletin 205, 339-350.
217. Schwarz, J., Weis, V. & Potts, D. (2002). Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima. Marine Biology 140, 471-478.
218. Shick, J. M., Iglic, K., Wells, M. L., Trick, C. G., Doyle, J. & Dunlap, W. C. (2011). Responses to iron limitation in two colonies of Stylophora pistillata exposed to high temperature: implications for coral bleaching. Limnology and Oceanography 56, 813-828.
219. Spalding, M. D., Green, E. P. & Ravilious, C. (2001). World Atlas of Coral Reefs University of California Press, Berkeley.
220. Stambler, N. (2011a). Marine microralgae/cyanobacteria - invertebrate symbiosis, trading energy for strategic material. In All Flesh is Grass: Plant-Animal Interactions (Volume 16, eds J. Seckbach and Z. Dubinsky), pp. 383-414.
221. Stambler, N. (2011b). Zooxanthellae: the yellow symbionts inside animals. In Coral Reefs: An Ecosystem in Transition (ed. S. N. Dubinsky Z), pp. 87-106. Springer, New York.
222. Stanley, G. D. Jr (2006). Photosymbiosis and the evolution of modern coral reefs. Science 312, 857-858.
223. Stanley, S. M. & Hardie, L. A. (1998). Secular oscillations in the carbonate mineralogy of reef-building and sediment-producing organisms driven by tectonically forced shifts in seawater chemistry. Palaeogeography Palaeoclimatology Palaeoecology 144, 3-19.
224. Stanley, S. M., Ries, J. B. & Hardie, L. A. (2002). Low-magnesium calcite produced by coralline algae in seawater of Late Cretaceous composition. Proceedings of the National Academy of Sciences 99, 15323-15326.
225. Stanley, S. M. & Swart, P. K. (1994). Evolution of the coral-zooxanthellae symbiosis during the Triassic: a geochemical approach. Paleobiology 21, 179-199.
226. Stat, M., Carter, D. & Hoegh-Guldberg, O. (2006). The evolutionary history of Symbiodinium and scleractinian hosts-Symbiosis, diversity, and the effect of climate change. Perspectives in Plant Ecology Evolution and Systematics 8, 23-43.
227. Stat, M., Morris, E. & Gates, R. D. (2008). Functional diversity in coral-dinoflagellate symbiosis. Proceedings of the National Academy of Sciences 105, 9256-9261.
228. Statham, P. J., Yeats, P. A. & Landing, W. M. (1998). Manganese in the eastern Atlantic Ocean: processes influencing deep and surface water distributions. Marine Chemistry 61, 55-68.
229. Stebbins, C. E. & Galán, J. E. (2001). Structural mimicry in bacterial virulence. Nature 412, 701-705.
230. Stoecker, D. K., Johnson, M. D., de Vargas, C. & Not, F. (2009). Acquired phototrophy in aquatic protists. Aquatic Microbial Ecology 57, 279-310.
231. Street, J. H. & Paytan, A. (2005). Iron, phytoplankton growth and the carbon cycle. Biogeochemical Cycles of Elements 43, 153-193.
232. Stuart, L. M., Boulais, J., Charriere, G. M., Hennessy, E. J., Brunet, S., Jutras, I., Goyette, G., Rondeau, C., Letarte, S., Huang, H., Ye, P., Morales, F., Kocks, C., Bader, J. S., Desjardins, M. & Ezekowitz, R. A. B. (2007). A systems biology analysis of the Drosophila phagosome. Nature 445, 95-101.
233. Stuart, L. M. & Ezekowitz, R. A. (2008). Phagocytosis and comparative innate immunity: learning on the fly. Nature Reviews Immunology 8, 131-141.
234. Sunagawa, S., Wilson, E. C., Thaler, M., Smith, M. L., Caruso, C., Pringle, J. R., Weis, V. M., Medina, M. & Schwarz, J. A. (2009). Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10, 258.
235. Swanson, R. & Hoegh-Guldberg, O. (1998). Amino acid synthesis in the symbiotic sea anemone Aiptasia pulchella. Marine Biology 131, 83-93.
236. Tchernov, D., Gorbunov, M. Y., de Vargas, C., Narayan Yadav, S., Milligan, A. J., Häggblom, M. & Falkowski, P. G. (2004). Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academy of Sciences 101, 13531-13535.
237. Thornhill, D. J., Daniel, M. W., LaJeunesse, T. C., Schmidt, G. W. & Fitt, W. K. (2006a). Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. Journal of Experimental Marine Biology and Ecology 338, 50-56.
238. Thornhill, D. J., Fitt, W. K. & Schmidt, G. W. (2006b). Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25, 515-519.
239. Thornhill, D., LaJeunesse, T., Kemp, D., Fitt, W. & Schmidt, G. (2006c). Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology 148, 711-722.
240. Thornhill, D. J., Xiang, Y., Fitt, W. K. & Santos, S. R. (2009). Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS ONE 4, e6262.
241. Titlyanov, E., Titlyanova, T., Leletkin, V., Tsukahara, J., vanWoesik, R. & Yamazato, K. (1996). Degradation of zooxanthellae and regulation of their density in hermatypic corals. Marine Ecology-Progress Series 139, 167-178.
242. Toller, W. W., Rowan, R. & Knowlton, N. (2001a). Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biological Bulletin 201, 360-373.
243. Toller, W. W., Rowan, R. & Knowlton, N. (2001b). Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biological Bulletin 201, 348-359.
244. Trench, R. (1993). Microalgal-Invertebrate Symbioses - a Review. Endocytobiosis and Cell Research 9, 135-175.
245. 14C by zooxanthellae in vitro. Proceedings of the Royal Society B: Biological Sciences 177, 237-250.
246. Trench, R. K. (1971b). 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 Sciences 177, 251-264.
247. Trench, R. K. (1987). Dinoflagellates in non-parasitic symbioses. In The Biology of Dinoflagellates (ed. F. J. R. Taylor), pp. 530-570. Blackwell, Oxford.
248. Turro, N. J., Ramamurthy, V. & Scaiano, J. C. (2009). Principles of Molecular Photochemistry: An Introduction University Science Books, Sausalito, CA.
249. Ulstrup, K. E., Kuhl, M. & Bourne, D. G. (2007). Zooxanthellae harvested by ciliates associated with brown band syndrome of corals remain photosynthetically competent. Applied and Environmental Microbiology 73, 1968-1975.
250. Ulstrup, K. E. & van Oppen, M. J. H. (2003). Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Molecular Ecology 12, 3477-3484.
251. Vacelet, J. (1981). Algal-sponge symbioses in the coral reefs of New Caledonia: morphological study. Proceedings of the 4th International Coral Reef Symposium, Manila, Philippines, Volume 2, pp. 713-719.
252. Venn, A. A., Loram, J. E. & Douglas A. E. (2008). Photosynthetic symbioses in animals. Journal of Experimental Botany 59, 1069-1080.
253. Veron, J. E. N. (1995). Corals in Space and Time: The Biogeography and Evolution of the Scleractinia. Cornell University Press, Ithaca.
254. Vianna, A. L. (1975). Interaction of calcium and magnesium in activating and inhibiting nucleoside triphosphatase of sarcoplasmic-reticulum vesicles. Biochimica et Biophysica Acta 410, 389-406.
255. de Villiers, S. (1998). Excess dissolved Ca in the deep ocean: a hydrothermal hypothesis. Earth and Planetary Science Letters 164, 627-641.
256. Wagner, D., Pochon, X., Irwin, L., Toonen, R. J. & Gates, R. D. (2011). Azooxanthellate? Most Hawaiian black corals contain Symbiodinium. Proceedings of the Royal Society B: Biological Sciences 278, 1323-1328.
257. Wakefield, T. S. & Kempf, S. C. (2001). Development of host- and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biological Bulletin 200, 127-143.
258. Waldron, K. J., Rutherford, J. C., Ford, D. & Robinson, N. J. (2009). Metalloproteins and metal sensing. Nature 460, 823-830.
259. Warner, M., Fitt, W. & Schmidt, G. (1999). Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proceedings of the National Academy of Sciences 96, 8007-8012.
260. Warner, M. E., LaJeunesse, T. C., Robison, J. D. & Thur, R. M. (2006). The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnology and Oceanography 51, 1887-1897.
261. Weis, V. M., Davy, S. K., Hoegh-Guldberg, O., Rodriguez-Lanetty, M. & Pringe, J. R. (2008). Cell biology in model systems as the key to understanding corals. Trends in Ecology & Evolution 23, 369-376.
262. Weisz, J., Massaro, A., Ramsby, B. & Hill, M. (2010). Zooxanthellar symbionts shape host sponge trophic status through translocation of carbon. Biological Bulletin 219, 189-197.
263. Wilcox, T. (1998). Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny. Molecular Phylogenetics and Evolution 10, 436-448.
264. Wilson, H. D., Schedl, H. P. & Christensen, K. (1989). Calcium-uptake by brush-border membrane-vesicles from the rat intestine. American Journal of Physiology 257, 446-453.
265. Wooldridge, S. A. (2010). Is the coral-algae symbiosis really 'mutually beneficial' for the partners? Bioessays 32, 615-625.
266. Yacobovitch, T., Benayahu, Y. & Weis, V. (2004). Motility of zooxanthellae isolated from the Red Sea soft coral Heteroxenia fuscescens (Cnidaria). Journal of Experimental Marine Biology and Ecology 298, 35-48.
267. Yamashita, H., Suzuki, G., Hayashibara, T. & Koike, K. (2011). Do corals select zooxanthellae by alternative discharge? Marine Biology 158, 87-100.
268. Yellowlees, D., Rees, T. A. V. & Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell and Environment 31, 679-694.
269. Zundelevich, A., Lazar, B. & Ilan, M. (2007). Chemical versus mechanical bioerosion of coral reefs by boring sponges-lessons from Pione cf. vastifica. Journal of Experimental Biology 210, 91-96.