Coral host transcriptomic states are correlated with Symbiodinium genotypes

Molecular Ecology

Volumn 19, Issue 6, 2010, Pages 1174-1186

  DeSalvo, M K ^a   Sunagawa, S ^a   Fisher, P L ^b   Voolstra, C R ^a,b   Iglesias Prieto, R ^c   Medina, M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Coral bleaching; Gene expression; Microarray; Symbiodinium; Thermal stress

Indexed keywords

ACCLIMATIZATION; ANIMAL; ANTHOZOA; ARTICLE; CLASSIFICATION; DINOFLAGELLATE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; GENOTYPE; HEAT; PHYSIOLOGY; SYMBIOSIS;

ACCLIMATIZATION; ANIMALS; ANTHOZOA; DINOFLAGELLIDA; GENE EXPRESSION PROFILING; GENOTYPE; HOT TEMPERATURE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SYMBIOSIS;

ANTHOZOA; DINOPHYCEAE; MONTASTRAEA FAVEOLATA; SYMBIODINIUM;

EID: 77950247237     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2010.04534.x     Document Type: Article

References (57)

1. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology Evolution and Systematics, 34, 661-689.
2. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals' adaptive response to climate change. Nature, 430, 741.
3. Bay LK, Ulstrup KE, Nielsen HB et al (2009) Microarray analysis reveals transcriptional plasticity in the reef building coral Acropora millepora. Molecular Ecology, 18, 3062-3075.
4. Berkelmans R, van Oppen MJ (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 Biological Sciences, 273, 2305-2312.
5. Bhagooli R, Hidaka M (2003) Comparison of stress susceptibility of in hospite and isolated zooxanthellae among five coral species. Journal of Experimental Marine Biology and Ecology, 291, 181-197.
6. Brown BE, Dunne RP, Goodson MS, Douglas AE (2002) Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs, 21, 119-126.
7. Bruno JF, Selig ER, Casey KS et al. (2007) Thermal stress and coral cover as drivers of coral disease outbreaks. PLoS Biology, 5, e124.
8. Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs, 28, 405-414.
9. Carpenter KE, Abrar M, Aeby G et al (2008) One-third of reefbuilding corals face elevated extinction risk from climate change and local impacts. Science, 321, 560-563.
10. Chun CK, Troll JV, Koroleva I et al (2008) Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proceedings of the National Academic Sciences, USA, 105, 11323-11328.
11. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist, 156, 19-34.
12. DeSalvo MK, Voolstra CR, Sunagawa S et al (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Molecular Ecology, 17, 3952-3971.
13. Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity, 81, 599-603.
14. Frade PR, De Jongh F, Vermeulen F, Van Bleijswijk J, Bak RPM (2008) Variation in symbiont distribution between closely related coral species over large depth ranges. Molecular Ecology, 17, 691-703.
15. Goulet TL (2006) Most corals may not change their symbionts. Marine Ecology-Progress Series, 321, 1-7.
16. Goulet TL, Cook CB, Goulet D (2005) Effect of short-term exposure to elevated temperatures and light levels on photosynthesis of different host-symbiont combinations in the Aiptasia pallidal Symbiodinium symbiosis. Limnology and Oceanography, 50, 1490-1498.
17. Grasso LC, Maindonald J, Rudd S et al. (2008) Microarray analysis identifies candidate genes for key roles in coral development. BMC Genomics, 9, 540.
18. Harvell CD, Mitchell CE, Ward JR et al (2002) Climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158-2162.
19. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Journal of Marine and Freshwater Research, 50, 839-866.
20. Hooper LV, Wong MH, Thelin A et al (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science, 291, 881-884.
21. Hughes TP, Baird AH, Bellwood DR et al. (2003) Climate change, human impacts, and the resilience of coral reefs. Science, 301, 929-933.
22. Iglesias-Prieto R, Beltran VH, 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 Biological Science, 271, 1757-1763.
23. 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 B: Biological Sciences, 275, 1359-1365.
24. Kinzie RA, Chee GS (1979) Effect of different zooxanthellae on the growth of experimentally re-infected hosts. Biological Bulletin, 156, 315-327.
25. Kitano H, Oda K (2006) Self-extending symbiosis: a mechanism for increasing robustness through evolution. Biologial Theory, 1, 61-66.
26. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biological Bulletin, 199, 126-134.
27. LaJeunesse TC, Reyes-Bonilla H, Warner ME (2007) Spring "bleaching" among Pocillopora in the Sea of Cortez, Eastern Pacific. Coral Reefs, 26, 265-270.
28. Little AF, van Oppen MJ, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science, 304, 1492-1494.
29. Loram JE, Trapido-Rosenthal HG, Douglas AE (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Molecular Ecology, 16, 4849-4857.
30. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. Journal of Experimental Biology, 211, 1050-1056.
31. Mieog JC, van Oppen MJH, Cantin NE, 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.
32. Mieog JC, Olsen JL, Berkelmans R et al. (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS ONE, 4, e6364.
33. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Ecosystems of the world 25: Coral Reefs (ed. Dubinsky Z), pp. 75-87. Elsevier, Amsterdam.
34. Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phytogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Molecular Phylogenetics and Evolution, 38, 20-30.
35. Reyes-Bermudez A, DeSalvo MK, Voolstra CR et al (2009) Gene expression microarray analysis encompassing metamorphosis and the onset of calcification in the scleractinian coral Montastraea faveolata. Marine Genomics, 2, 149-159.
36. Richier S, Rodriguez-Lanetty M, Schnitzler CE, Weis VM (2008) Response of the symbiotic cnidarian Anthopleura elegantissima transcriptome to temperature and UV increase. Comparative Biochemistry and Physiology D: Genomics Proteomics, 3, 283-289.
37. 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.
38. Rodriguez-Roman A, Hernandez-Pech X, Thome PE, Enriquez S, Iglesias-Prieto R (2006) Photosynthesis and light utilization in the Caribbean coral Montastraea faveolata recovering from a bleaching event. Limnology and Oceanography, 51, 2702-2710.
39. Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature, 430, 742.
40. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proceedings of National Academic Sciences, USA, 92, 2850-2853.
41. Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Marine Ecology-Progress Series, 71, 65-73.
42. Rowan R, Knowlton N, Baker AC, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature, 388, 265-269.
43. Saeed AI, Sharov V, White J et al (2003) TM4: a free, open-source system for microarray data management and analysis. BioTechniques, 34, 374-378.
44. 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 Academic Sciences, USA, 105, 10444-10449.
45. Severance EG, Szmant AM, Karl SA (2004) Microsatellite loci isolated from the Caribbean coral, Montastraea annularis. Molecular Ecology Notes, 4, 74-76.
46. 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.
47. Stat M, Morris E, Gates RD (2008) Functional diversity in coraldinoflagellate symbiosis. Proceedings of the National Academuc Sciences of the USA, 105, 9256-9261.
48. Sunagawa S, Desantis TZ, Piceno YM et al. (2009) Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. Isme Journal, 3, 512-521.
49. Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics, 22, 1540-1542.
50. Tchernov D, Gorbunov MY, de Vargas C et al (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academic Sciences, USA, 101, 13531-13535.
51. The-UniProt-Consortium (2008) The Universal Protein Resource (UniProt). Nucleic Acids Research, 36, D190-D195.
52. Thornhill DJ, Lajeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology, 148, 711-722.
53. Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biology Bulletin, 201, 348-359.
54. Townsend JP, Hartl DL (2002) Bayesian analysis of gene expression levels: statistical quantification of relative mRNA level across multiple strains or treatments. Genome Biology, 3, RESEARCH0071.
55. Voolstra CR, Schwarz JA, Schnetzer J et al. (2009) The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Molecular Ecology, 18, 1823-1833.
56. Warner ME, LaJeunesse TC, Robison JD, Thur RM (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.
57. Zheng Q, Wang XJ (2008) GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Research, 36, W358-W363.