Niche partitioning of closely related symbiotic dinoflagellates

Molecular Ecology

Volumn 16, Issue 17, 2007, Pages 3721-3733

  Sampayo, Eugenia M ^a   Franceschinis, Lorenzo ^a,b   Hoegh Guldberg, Ove ^a   Dove, Sophie ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF BREMEN   (Germany)

Author keywords

Ecology; Pocillopora; Seriatopora; Stylophora; Symbiodinium ITS2; Zonation

Indexed keywords

RIBOSOMAL SPACER DNA;

ANIMAL; ANTHOZOA; ARTICLE; AUSTRALIA; CHEMISTRY; CLASSIFICATION; DINOFLAGELLATE; DNA SEQUENCE; ECOSYSTEM; GENETICS; MULTIVARIATE ANALYSIS; PHYLOGENY; PHYSIOLOGY; SYMBIOSIS;

ANIMALS; ANTHOZOA; AUSTRALIA; DINOFLAGELLIDA; DNA, RIBOSOMAL SPACER; ECOSYSTEM; MULTIVARIATE ANALYSIS; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

ANTHOZOA; DINOPHYCEAE; POCILLOPORA; POCILLOPORA DAMICORNIS; SERIATOPORA; SERIATOPORA HYSTRIX; STYLOPHORA (CORAL); STYLOPHORA PISTILLATA; SYMBIODINIUM;

EID: 34548533977     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2007.03403.x     Document Type: Article

References (82)

1. Apprill AM, Gates RD (2007) Recognizing diversity in coral symbiotic dinoflagellate communities. Molecular Ecology, online first: doi: 10.1111/j.1365-294X.2006.03214.x.
2. Baille BK, Belda-Baille CA, Maruyama T (2000) Conspecificity and Indo-Pacific distribution of symbiodinium genotypes (Dinophyceae) from giant clams. Journal of Phycology, 36, 1153 1161.
3. Baker AC (1999) The symbiosis ecology of reef-building corals. PhD Thesis, Rosenthiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida.
4. Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean acroporid corals. Proceedings 8th International Coral Reef Symposium, Panama, 2, 1295 1300.
5. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals' adaptive response to climate change. Nature, 430, 741 741.
6. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for corals reefs in an era of climate change. Proceeding of the Royal Society of London. Series B, Biological Sciences, 273, 2305 2312.
7. Blank RJ, Trench RK (1985) Speciation and symbiotic dinoflagellates. Science, 229, 656 658.
8. Buckler SE, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics, 145, 821 832.
9. Burnett WJ (2002) Longitudinal variation in algal symbionts (zooxanthellae) from the Indian Ocean zoanthid Palythoa caesia. Marine Ecology Progress Series, 234, 105 109.
10. Chang SS, Prezelin BB, Trench RK (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Marine Biology, 76, 219 229.
11. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology, 18, 117 143.
12. Clement M, Posada D, Crandall KA (2001) tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9 (10 1657 1659.
13. Cohan FM (2001) Bacterial species and speciation. Systematic Biology, 50, 513 524.
14. Cohan FM (2002) What are bacterial species? Annual Reviews in Microbiology, 56, 457 487.
15. DeLong EF, Pace NR (2001) Environmental diversity of bacteria and archaea. Systematic Biology, 50 (4 470 478.
16. Diekmann OE, Bak RPM, Tonk L, Stam WT, Olsen JL (2002) No habitat correlation of zooxanthellae in the coral genus Madracis on a Curacao reef. Marine Ecology Progress Series, 227, 221 232.
17. Dove S, Ortiz JC, Enriquez S et al 2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnology and Oceanography, 51 (2 1149 1158.
18. Duineveld BM, Kowalchuk GA, Keijzer A, van Elsas JD, van Veen JA (2001) Analysis of bacterial communities in the rhizosphere of Chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Applied and Environmental Microbiology, 67 (1 172 178.
19. Enriquez S, Mendez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnology and Oceanography, 50, 1025 1032.
20. Ferris MJ, Kuhl M, Wieland A, Ward DM (2003) Cyanobacterial ecotypes in different optical microenvironments of a 68 °C hot spring mat community revealed by 16S-23S rRNA Internal Transcribed Spacer region variation. Applied and Environmental Microbiology, 69 (5 2893 2898.
21. Finlay BJ, Fenchel T (2004) Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist, 155, 237 244.
22. Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov, a zooxanthella: taxonomy, life cycle and morphology. Journal of Protozoology, 9, 45 53.
23. Goulet TL (2006) Most corals may not change their symbionts. Marine Ecology Progress Series, 321, 1 7.
24. Goulet TL, Coffroth MA (2003) Genetic composition of zooxanthellae between and within colonies of the octocoral Plexaura kuna, based on small subunit rDNA and multilocus DNA fingerprinting. Marine Biology, 142, 233 239.
25. Hodkinson TR, Renvoize SA, Chonghaile GN, Stapleton CMA, Chase MW (2000) A comparison of ITS nuclear rDNA sequence data and AFLP markers for phylogenetic studies in Phyllostachys (Bambusoideae, Poaceae). Journal of Plant Research, 113, 259 269.
26. Hughes TP, Baird AH, Bellwood DR et al 2003) Climate change, human impacts, and the resilience of coral reefs. Science, 301, 929 933.
27. Hunter CL, Morden CW, Smith CM (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. Proceedings of the 8th international Coral Reef Symposium. Panama, 2, 1599 1602.
28. 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 the Royal Society of London. Series B, Biological Sciences, 271, 1757 1763.
29. Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Marine Ecology Progress Series, 113, 163 175.
30. Iglesias-Prieto R, Trench RK (1997a) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Marine Biology, 130, 23 33.
31. Iglesias-Prieto R, Trench RK (1997b) Photoadaptation, photoacclimation and niche diversification in invertebrate-dinoflagellate symbiosis. Proceedings of the 8th International Coral Reef Symposium, Panama, 2, 1319 1324.
32. Janse I, Bok J, Zwart G (2004) A simple remedy against artifactual double bands in denaturing gradient gel electrophoresis. Journal of Microbiological Methods, 57, 279 281.
33. Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward EMS, Chisholm SW (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science, 311, 1737 1740.
34. LaJeunesse TC (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 (5 866 880.
35. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology, 141 (2 387 400.
36. LaJeunesse TC (2005) Species radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Molecular Biology and Evolution, 22 (3 570 581.
37. LaJeunesse TC, Bhagooli R, Hidaka M et al 2004a) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology Progress Series, 284, 147 161.
38. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnology and Oceanography, 48 (5 2046 2054.
39. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004b) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs, 23 (4 596 603.
40. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biological Bulletin, 199 (2 126 134.
41. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Nature, 304, 1492 1494.
42. Loh WKW, Loi T, Carter D, Hoegh-Guldberg O (2001) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Marine Ecology Progress Series, 222, 97 107.
43. Moreira D, López-García P (2002) The molecular ecology of microbial eukaryotes unveils a hidden world. Trends in Microbiology, 10 (1 31 38.
44. Muyzer GM (1999) DGGE/TGGE: a method for identifying genes from natural ecosystems. Current Opinion in Microbiology, 2 (3 317 322.
45. van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Molecular Ecology, 15 (13 3863 3854.
46. van Oppen MJH, Palstra FP, Piquet AMT, Miller D (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.
47. Palys T, Cohan FM, Nakamura LK (1997) Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. International Journal of Systematic Bacteriology, 47, 1145 1156.
48. Pfiester LA, Anderson DM (1987) Dinoflagellate reproduction. In : The Biology of Dinoflagellates (ed. Taylor FRJ), pp. 611 648. Blackwell Scientific Publications, London.
49. Quinn JP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK.
50. Ramsing NB, Ferris MJ, Ward DM (2000) Highly ordered vertical structure of Synechococcus populations within the one-millimeter-thick photic zone of a hot spring cyanobacterial mat. Applied and Environmental Microbiology, 66, 1038 1049.
51. Rodriguez-Lanetty M (2003) Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA. Molecular Phylogenetics and Evolution, 28 (1 152 168.
52. Rodriguez-Lanetty M, Chang SJ, Song JI (2003) Specificity of two temperate dinoflagellate-anthozoan associations from the north-western Pacific Ocean. Marine Biology, 143 (6 1193 1199.
53. Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Guldberg O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Marine Biology, 138 (6 1175 1181.
54. Rowan R (2004) Coral bleaching - thermal adaptation in reef coral symbionts. Nature, 430, 742 742.
55. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proceedings of the National Academy of Sciences, USA, 92 (7 2850 2853.
56. 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.
57. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science, 251, 1348 1351.
58. Santos SR, Coffroth MA (2003) Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium are haploid. Biological Bulletin, 204, 10 20.
59. Santos SR, Gutierrez-Rodriguez C, Lasker HR, Coffroth MA (2003) Symbiodinium sp. associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates. Marine Biology, 143 (1 111 120.
60. Santos SR, Taylor DJ, Kinzie RA, Sakai K, Coffroth MA (2002) Evolution of length variation and heteroplasmy in the chloroplast rDNA of symbiotic dinoflagellates (Symbiodinium, Dinophyta) and a novel insertion in the universal core region of the large subunit rDNA. Phycologia, 41 (4 311 318.
61. Savage AM, Trapido-Rosenthal H, Douglas AE (2002) On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Marine Ecology Progress Series, 244, 27 37.
62. Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (=Gymniodinium) microadriaticum Freudenthal, and its specificity in its symbiosis with marine invertebrates. I. Isoenzyme and soluble protein patterns of axenic cultures of Symbiodinium microadriaticum. Proceedings of the Royal Society of London, Series B, Biological Sciences, 207, 405 427.
63. Sekiguchi H, Tomioka N, Nakahara T, Uchiyama H (2001) A single band does not always represent single bacterial strains in denaturing gradient gel electrophoresis analysis. Biotechnology Letters, 23 (15 1205 1208.
64. Sekiguchi H, Watanabe M, Nakahara T, Xu B, Uchiyama H (2002) Succession of bacterial community structure along the Changjiang River determined by denaturing gradient gel electrophoresis and clone library analysis. Applied and Environmental Microbiology, 68 (10 5142 5150.
65. Speksnijder A, Kowalchuk GA, De Jong S, Kline E, Stephen JR, Laanbroek HJ (2001) Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Applied and Environmental Microbiology, 67 (1 469 472.
66. Stamper DM, Walch M, Jacobs RN (2003) Bacterial population changes in a membrane bioreactor for graywater treatment monitored by denaturing gradient gel electrophoretic analysis of 16S rRNA gene fragments. Applied and Environmental Microbiology, 69 (2 852 860.
67. Stoeck T, Epstein S (2003) Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Applied and Environmental Microbiology, 69 (5 2657 2663.
68. Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). Journal of Phycology, 40 (1 160 164.
69. 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 Academy of Sciences, USA, 101 (37 13531 13535.
70. Templeton AR (1989) The meaning of species and speciation: a genetic perspective. In : Speciation and its Consequences (eds Otte D, Endler JA pp. 3 27. Sinauer Associates, Sunderland, Massachusetts.
71. Templeton AR (1994) The role of molecular genetics in speciation. In : Molecular Ecology and Evolution: Approaches and Applications (eds Schierwater B, Streit B, Wagner GP, DeSalle R), pp. 455 477. Birkhäuser Verslag, Basel, Switzerland.
72. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. 111. Cladogram estimation. Genetics, 132, 619 633.
73. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The clustal_x Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876 4882.
74. 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.
75. 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. Biological Bulletin, 201, 248 359.
76. Trench RK, Blank RJ (1987) Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov. gymnodinioid dinoflagellate symbionts of marine invertebrates. Journal of Phycology, 23, 469 481.
77. 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.
78. van Valen L (1976) Ecological species, multispecies, and oaks. Taxon, 25, 233 239.
79. Wang Q, Deeds JR, Place AR, Belas R (2004) Dinoflagellate community analysis of a fish kill using denaturant gradient gel electrophoresis. Harmful Algae, 4 (1 151 162.
80. Warner M, Fitt WK, Schmidt GW (1999) Damage to photosystem II in dinoflagellates: a determinant of coral bleaching. Proceedings of the National Academy of Sciences, USA, 96, 8007 8012.
81. Warner ME, LaJeunesse TC, Robison JE, 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 (4 1887 1897.
82. Wiley EO (1978) The evolutionary species concept reconsidered. Systematic Zoology, 27 (1 17 26.