Phylogenetic relationships among zooxanthellae (Symbiodinium) associated to excavating sponges (Cliona spp.) reveal an unexpected lineage in the Caribbean

Molecular Phylogenetics and Evolution

Volumn 49, Issue 2, 2008, Pages 554-560

  Granados, C ^a   Camargo, C ^a   Zea, S ^b   Sanchez J A ^a  

^a UNIVERSIDAD DE LOS ANDES   (Colombia)

^b UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

Caribbean; Clade G; Cliona; Excavating sponges; Symbiodinium; Zooxanthellae

Indexed keywords

CHLOROPLAST DNA; PROTOZOAL DNA; RIBOSOMAL SPACER DNA; RNA 18S;

ANIMAL; ARTICLE; BAYES THEOREM; CENTRAL AMERICA; CLASSIFICATION; DINOFLAGELLATE; DNA SEQUENCE; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; PHYSIOLOGY; SEQUENCE ALIGNMENT; SPONGE (PORIFERA); STATISTICAL MODEL; SYMBIOSIS;

ANIMALS; BAYES THEOREM; CARIBBEAN REGION; DINOFLAGELLIDA; DNA, CHLOROPLAST; DNA, PROTOZOAN; DNA, RIBOSOMAL SPACER; EVOLUTION, MOLECULAR; LIKELIHOOD FUNCTIONS; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 18S; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

ALGAE; CLIONA; CLIONA APRICA; CLIONA CARIBBAEA; CLIONA TENUIS; CNIDARIA; DINOPHYCEAE; SYMBIODINIUM;

EID: 55049107227     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2008.07.023     Document Type: Article

References (68)

1. Baker A.C. Reef corals bleach to survive change. Nature 411 (2001) 765-766
2. Baker A.C. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34 (2003) 661-689
3. Bellwood D.R., Hughes T.P., Folke C., and Nystroem M. Confronting the coral reef crisis. Nature 429 (2004) 827-833
4. Berkelmans R., and van Oppen M.J.H. The role of zooxanthellae in the thermal tolerance of corals: a "nugget of hope" for coral reefs in an era of climate change. Proc. R. Soc. Lond. B 273 (2006) 2305-2312
5. Carlos A.A., Baillie B.K., Kawachi M., and Maruyama T. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J. Phycol. 35 (1999) 1054-1062
6. Coffroth M.A., Lasker H.R., Diamond M.E., Bruenn J.A., and Bermingham E. DNA fingerprints of a gorgonian coral: a method for detecting clonal structure in a vegetative species. Mar. Biol. 114 (1992) 317-325
7. Coffroth M.A., Santos S.R., and Goulet T. Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar. Ecol. Prog. Ser. 222 (2001) 85-96
8. Coleman A.W. ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends Genet. 19 (2003) 370-375
9. Coleman A.W. Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Res. 35 (2007) 3322-3329
10. Coleman A.W., Suarez A., and Goff L.J. Molecular delineation of species and syngens in Volvocean green algae (Clorophyta). J. Phycol. 30 (1994) 80-90
11. Denboh T., Ichimura T., Hendrayanti D., and Coleman A.W. Closterium moniliferum-ehrenbergii (Charophyceae, Chlorophyta) species complex viewed from 1506 group I intron and ITS2 of nuclear rDNA. J. Phycol. 39 (2003) 960-977
12. DeRijk P., and De Wachter R. RnaViz, a program for the visualisation of RNA secondary structure. Nucleic Acids Res. 25 (1997) 4679-4684
13. Díaz M.C., and Rützler K. Sponges: an essential component of Caribbean coral reefs. Bull. Mar. Sci. 69 (2001) 535-546
14. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5 (2004) 113
15. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985) 783-791
16. Garren M., Walsh S., Caccone A., and Knowlton N. Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 25 (2006) 503-512
17. Garson M.J., Flowers A.E., Webb R.I., Charan R.D., and McCaffrey E.J. A sponge/dinoflagellate association in the haplosclerid sponge Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation. Cell Tissue Res. 293 (1998) 365-373
18. Glynn P. Bioerosion and coral-reef growth; a dynamic balance. Life and death of coral reefs (1997), Chapman and Hall, New York pp. 68-95
19. Gottschling M., and Plotner J. Secondary structure models of the nuclear internal transcribed spacer regions and 5.8S rRNA in Calciodinelloideae (Peridiniaceae) and other dinoflagellates. Nucleic Acids Res. 32 (2004) 307-315
20. Goulet T. Most corals may not change their symbionts. Mar. Ecol. Prog. Ser. 321 (2006) 1-7
21. Goulet T., and Coffroth M.A. The genetic identity of dinoflagellate symbionts in Caribbean octocorals. Coral Reefs 23 (2004) 465-472
22. Goulet T., Simmons C., and Goulet D. Worldwide biogeography of Symbiodinium in tropical octocorals. Mar. Ecol. Prog. Ser. 355 (2008) 45-58
23. Hill M.S. Symbiotic zooxanthellae enhance boring and growth rates of the tropical sponge Anthosigmella varians forma varians. Mar. Biol. 125 (1996) 649-654
24. Hill M.S., and Wilcox T. Unusual mode of symbiont repopulation after bleaching in Anthosigmella varians: acquisition of different zooxanthellae strains. Symbiosis 25 (1998) 279-289
25. Holmes K.E. Effects of eutrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae). Invertebr. Biol. 119 (2000) 125-138
26. Huelsenbeck J.P., and Ronquist F. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
27. Hunter R.L., LaJeunesse T.C., and Santos S.R. Structure and evolution of the rDNA internal transcribed spacer (ITS) region 2 in the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J. Phycol. 43 (2007) 120-128
28. Joseph N., Krauskopf E., Vera M.I., and Michot B. Ribosomal internal transcribed spacer 2 (ITS2) exhibits a common core of secondary structure in vertebrates and yeast. Nucleic Acids Res. 27 (1999) 4533-4540
29. LaJeunesse T.C. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates of the genus Symbiodinium using the ITS region: in search of a 'species' level marker. J. Phycol. 37 (2001) 866-880
30. LaJeunesse T.C. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar. Biol. 141 (2002) 387-400
31. LaJeunesse T.C. "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol. Biol. Evol. 22 (2005) 570-581
32. LaJeunesse T.C., Loh W.K.W., van Woesik R., Hoegh-Guldberg O., Schmidt G.W., and Fitt W.K. Low symbiont diversity in southern great barrier reef corals, relative to those of the Caribbean. Limnol. Oceanogr. 48 (2003) 2046-2054
33. López-Victoria M., and Zea S. Storm-mediated coral colonization by an excavating Caribbean sponge. Clim. Res. 26 (2004) 251-256
34. López-Victoria M., and Zea S. Current trends of space occupation by encrusting excavating sponges on Colombian coral reefs. Mar. Ecol. 26 (2005) 33-41
35. López-Victoria M., Zea S., and Weil E. Competition for space between encrusting excavating Caribbean sponges and other coral reef organisms. Mar. Ecol. Prog. Ser. 312 (2006) 113-121
36. Mai J.C., and Coleman A.W. The internal transcribed spacer 2 exhibits a common secondary structure in green algae and flowering plants. J. Mol. Evol. 44 (1997) 258-271
37. Pang, R., 1973. The systematics of some Jamaican excavating sponges (Porifera). Postilla.
38. Pawlowski J., Holzmann M., Fahrni J.F., Pochon X., and Lee J.J. Molecular identification of algal endosymbionts in large miliolid foraminifera: 2. Dinoflagellates. J. Eukaryot. Microbiol. 48 (2001) 368-373
39. Pochon X., Garcia-Cuetos L., Baker A.C., Castetlla E., and Pawlowski J. One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in Soritid foraminifera. Coral Reefs 26 (2007) 867-882
40. Pochon X., LaJeunesse T.C., and Pawlowski J. Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar. Biol. 146 (2004) 17-27
41. Pochon X., Montoya-Burgos J.I., Stadelmann B., and Pawlowski J. Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellates genus Symbiodinium. Mol. Phylogenet. Evol. 38 (2006) 20-30
42. Pochon X., Pawlowski J., Zaninetti L., and Rowan R. High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in Soritid foraminifera. Mar. Biol. 139 (2001) 1069-1078
43. Porto, I., Granados, C., Restrepo, J.C., Sánchez, J.A., 2008. Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS ONE 3, e2160. doi:10.1371/journal.pone.0002160.
44. Posada D., and Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
45. Reimer J.D., Ono S., Tsukahara J., Takishita K., and Maruyama T. Non-seasonal clade-specificity and subclade microvariation in symbiotic dinoflagellates (Symbiodinium spp.) in Zoanthus sansibaricus (Anthozoa: Hexacorallia) at Kagoshima Bay, Japan. Phycol. Res. 55 (2007) 58-65
46. Rose C., and Risk M. Increase in Cliona delitrix infestation of Montastraea cavernosa heads on an organically polluted portion of the Grand Cayman. Mar. Ecol. 6 (1985) 345-363
47. Rowan R. Diversity and ecology of zooxanthella on coral reefs. J. Phycol. 34 (1998) 407-417
48. Rowan R. Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430 (2004) 742
49. Rowan R., and Powers D.A. Ribosomal RNA sequences and the diversity of symbiotic dinoflagellates (zooxanthellae). Proc. R. Soc. Lond. B 89 (1992) 3639-3643
50. Rützler K. Associations between Caribbean sponges and photosynthetic organism. In: Rützler K. (Ed). New Perspectives in Sponge Biology (1990), Smithsonian Institution Press, Washington DC 455-466
51. Rützler K. Impact of crustose clionid sponges on Caribbean reef corals. Acta Geol. Hisp. 37 (2002) 61-72
52. Santos S.R., and Coffroth M.A. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156 (2005) 19-34
53. Santos S.R., Gutierrez-Rodriguez C., and Coffroth M.A. Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)-ribosomal DNA sequences. Mar. Biotechnol. 5 (2003) 130-140
54. Santos S.R., Taylor D.J., Kinzie R.A., Hidaka M., Sakai K., and Coffroth M.A. Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol. Phylogenet. Evol. 23 (2002) 97-111
55. Schönberg C. Sponges of the 'Cliona viridis complex'-a key species identification. Proc. 9th Int. Coral Reef Symp. Bali 1 (2002) 295-300
56. Schönberg C. Global environmental changes: boring sponges call for more attention. 7th Int. Sponge Symp. 1 (2006) 312
57. Schönberg C., and Loh W.K.W. Molecular identity of the unique symbiotic dinoflagellates found in the bioeroding demosponge Cliona orientalis. Mar. Ecol. Prog. Ser. 299 (2005) 157-166
58. Schönberg C., Suwa R., Hidaka M., and Loh W.K.W. Sponge and coral zooxanthellae in heat and light: preliminary results of photochemical efficiency monitored with pulse amplitude modulated fluorometry. Mar. Ecol. 29 (2008) 247-258
59. Schönberg C., and Wilkinson C. Induced colonization of coral by a clionid bioeroding sponge. Coral Reefs 20 (2001) 69-76
60. Stamatakis, A., Hovver, P., Rougemont, J., 2008. A rapid bootstrap algorithm for the RAxML web-servers. Syst. Biol., in press.
61. Steindler L., Beer S., Peretzman-Shemer A., Nyberg C., and Ilan M. Photoadaptation of zooxanthellae in the sponge Cliona vastifica from the Red Sea, as measured in situ. Mar. Biol. 138 (2001) 511-515
62. Swofford D.L. PAUP*, phylogenetic analysis using parsimony (* and other methods) (2002), Sinauer Associates, Sunderland
63. van Oppen M.J.H., Mieog J.C., Sánchez C.A., and Fabricius K.E. Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol. Ecol. 14 (2005) 2403-2417
64. Vicente V.P. An ecological evaluation of the West Indian demosponge Anthosigmella varians (Hadromerida: Spirastrellidae). Bull. Mar. Sci. 28 (1978) 771-777
65. Vicente V.P. Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8 (1990) 199-202
66. Walther G.R., Post E., Convey P., Menzel A., Parmesan C., Beebee T.J.C., Fromentin J.M., Hoegh-Guldberg O., and Bairlein F. Ecological responser to recent climate change. Nature 416 (2002) 389-395
67. Zea S., and Weil E. Taxonomy of the Caribbean excavating sponge species complex Cliona caribbaea-C. aprica-C. langae (Porifera, Hadromerida, Clionaidae). Caribb. J. Sci. 39 (2003) 348-370
68. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 (2003) 3406-3415