Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny

Molecular Ecology

Volumn 18, Issue 16, 2009, Pages 3532-3543

  Abrego, David ^a,b,c   Van Oppen, Madeleine J H ^c   Willis, Bette L ^a,b  

^a AIMS at JCU ^*  (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

^c AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Corals; Reproductive maturity; Specificity; Symbiodinium

Indexed keywords

ANIMAL; ANTHOZOA; ARTICLE; DINOFLAGELLATE; ECOSYSTEM; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE; SPECIES DIFFERENCE; SYMBIOSIS; TIME;

ANIMALS; ANTHOZOA; DINOFLAGELLIDA; ECOSYSTEM; LIFE CYCLE STAGES; SPECIES SPECIFICITY; SYMBIOSIS; TIME FACTORS;

ACROPORA; ACROPORA MILLEPORA; ACROPORA TENUIS; ALGAE; ANTHOZOA; DINOPHYCEAE; SYMBIODINIUM;

EID: 68349135371     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04276.x     Document Type: Article

References (43)

1. Abrego D, van Oppen MJH, Willis BL (2009) Highly infectious symbiont dominates initial uptake in coral juveniles. Molecular Ecology, 18, doi :.
2. Babcock RC, Bull GD, Harrison PL et al. (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Marine Biology, 90, 379 394.
3. Baker A (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution and Systematics, 34, 661 689.
4. Belda-Baillie CA, Baillie BA, Maruyama T (2002) Specificity of a model cnidarian-dinoflagellate symbiosis. Biological Bulletin, 202, 74.
5. Berkelmans R, van Oppen M (2006) The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proceedings of the Royal Society of London, Series B: Biological Sciences, 273, 2305 2312.
6. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist, 156, 19 34.
7. Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Marine Ecology Progress Series, 222, 85 96.
8. Davy SK, Lucas IAN, Turner JR (1997) Uptake and persistence of homologous and heterologous zooxanthellae in the temperate sea anemone Cereus pedunculatus (Pennant). Biological Bulletin, 192, 208.
9. Dunn SR, Weis VM (2009) Apoptosis as a post-phagocytic winnowing mechanism in a coral-dinoflagellate mutualism. Environmental Microbiology, 11, 269 276.
10. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Molecular Ecology, 13, 2445 2458.
11. Fitt WK (1985) Effect of different strains of the zooxanthella Symbiodinium microadriaticum on growth and survivial of their coelentrerate and molluscan hosts. Proceedings of the Fifth International Coral Reef Congress, 6, 131 136.
12. Gomez-Cabrera M, Ortiz J, Loh W, Ward S, Hoegh-Guldberg O (2008) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs, 27, 219 226.
13. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In : Coral Reef (ed. Dubinsky Z pp. 133 208. Elsevier, Amsterdam.
14. Iglesias-Prieto R, Beltran V, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings of the Royal Society of London, Series B: Biological Sciences, 271, 1757 1763.
15. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society of London, Series B: Biological Sciences, 275, 1359 1365.
16. Kinzie RA III., Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biological Bulletin, 200, 51 58.
17. Lin K-L, Wang J-T, Fang L-S (2000) Participation of glycoproteins on zooxanthellal cell walls in the establishment of a symbiotic relationship with the sea anemone, Aiptasia pulchella. Zoological Studies, 39, 172 178.
18. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science, 304, 1492 1494.
19. Mieog J, VanOppen MJH, Cantin N, Stam WT, Olsen JL (2007) Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs, 26, 449 457.
20. Nyholm SV, McFall-Ngai MJ (2004) The winnowing:establishing the squid-Vibrio symbiosis. Nature Reviews Microbiology, 2, 632 642.
21. van Oppen MJH, Palstra FP, Piquet A-T, Miller DJ (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proceedings of the Royal Society of London, Series B: Biological Sciences, 268, 1759 1767.
22. van Oppen M, Mahiny A, Done T (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.
23. Quinn G, Keough M (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.
24. Reynolds WS, Schwarz JA, Weis VM (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 - Part A: Molecular & Integrative Physiology, 126, 33 44.
25. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrohphyta). Journal of Phycology, 42, 568 579.
26. Rodriguez-Lanetty M, Krupp DA, Weis VM (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Marine Ecology Progress Series, 275, 97 102.
27. Rodriguez-Lanetty M, Phillips WS, Weis VM (2006) Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics, 7, 23.
28. Rodriguez-Roman A, Iglesias-Prieto R (2005) Regulation of photochemical activity in cultured symbiotic dinoflagellates under nitrate limitation and deprivation. Marine Biology, 146, 1063 1073.
29. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proceedings of the National Academy of Sciences, USA, 92, 2850 2853.
30. Sampayo EM, 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, USA, 105, 10 444 10 449.
31. Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biological Bulletin, 196, 70.
32. Schwarz JA, Weis VM, Potts DC (2002) Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima. Marine Biology, 140, 471 478.
33. Sokal RR, Rohlf JF (1996) Introduction to Biostatistics. WH Freeman and Company, New York.
34. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006a) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology, 148, 711 722.
35. Thornhill DJ, Daniel MW, LaJeunesse TC, Schmidt GW, Fitt WK (2006b) Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. Journal of Experimental Marine Biology and Ecology, 338, 50 56.
36. Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease-associated bleaching. Biological Bulletin, 201, 360.
37. Ulstrup KE, van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Molecular Ecology, 12, 3477 3484.
38. Ulstrup KE, van Oppen MJH, Kuhl M, Ralph PJ (2007) Inter-polyp genetic and physiological characterisation of Symbiodinium in an Acropora valida colony. Marine Biology, 153, 225 234.
39. 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.
40. Willis BL, Babcock RC, Harrison PL, Oliver JK (1985) Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. Proceedings of Fifth International Coral Reef Congress, 4, 343 348.
41. Wilson K, Li Y, Whan V et al. (2002) Genetic mapping of the black tiger shrimp Penaeus monodon with amplified fragment length polymorphism. Aquaculture, 204, 297 309.
42. Wood-Charlson EM, Hollingsworth LH, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiology, 8, 1985 1994.
43. Yuyama I, Hayakawa H, Endo H et al. (2005) Identification of symbiotically expressed coral mRNAs using a model infection system. Biochemical and Biophysical Research Communications, 336, 793 798.