Abstract
Some marine animals have a dynamic mutualistic association involving heterotrophic coral animals (hosts) and autotrophic dinoflagellate endosymbionts in the genus Symbiodinium, known as zooxanthellae, which are directly involved in their physiology. Currently, there is limited knowledge of the Symbiodinium diversity associated with zoanthids from the Brazilian coast. Hence, this study assessed the diversity of zooxanthellae associated with Palythoa caribaeorum, Zoanthus sociatus and Protopalythoa variabilis commonly found on the northeast coast. Zoanthids samples were collected from sandstone reefs, and the total DNA from the samples was extracted. Diversity was assessed by denaturing gradient gel electrophoresis (DGGE) and ITS region cloning library. Data from ITS region sequences showed that zoanthids hosted two phylogenetic subclades or subgenus (C1 and A3) closely related to Symbiodinium from previous studies. Subclade C1 was found in Pa. caribaeorum, Pr. variabilis and Z. sociatus, while subclade A3 was found exclusively in Z. sociatus. This suggests that Pa. caribaeorum and Pr. variabilis are extremely selective, whereas Z. sociatus shows greater flexibility in the selection of its symbionts, and these differences may be involved with living in different reef environments. Knowledge of zooxanthellae diversity associated with zoanthids can explain their large distribution in Brazilian coast and contribute to a better understanding of zoanthid’s sensitivity to thermal stress.
Similar content being viewed by others
References
Allemand D, Furla P, Bénazet-Tambutte S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. C J Bot 76:925–941
Al-Utaibi AA, Niaz GR, Al-Lihaibi SS (2009) Mycosporine-like amino acids in six scleractinian coral species. Oceanologia 51:93–104
Annenkova NV, Lavrov DV, Belikova SI (2011) Dinoflagellates associated with freshwater sponges from the ancient Lake Baikal. Protist 162:222–236
Apprill AM, Gates RD (2007) Recognizing diversity in coral symbiotic dinoflagellate communities. Mol Ecol 16:1127–1134
Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766
Baker AC (2003) Flexibility and specificity in coral algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689
Banaszak AT, Lajeunesse TC, Trench RK (2000) The synthesis of mycosporine-like amino acids (MAAs) by cultured symbiotic dinoflagellates. J Exp Mar Biol Ecol 249:219–233
Bastidas C, Bone D (1996) Competitive strategies between Palythoa caribaeorum and Zoanthus sociatus (Cnidaria:Anthozoa) at a reef flat environmental in Venezuela. Bull Mar Sci 59:543–555
Baums IB, Johnson ME, Devlin-Durante MK, Miller MW (2010) Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean. Coral Reefs 29:835–842
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. Proc Biol Sci 273:2305–2312
Burghardt I, Stemmera K, Wägele H (2008) Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca: Gastropoda), with analyses of long-term retention. Org Divers Evol 8:66–76
Burnett JW (2002) Longitudinal variation in algal symbionts (zooxanthellae) from the Indian Ocean zoanthid Palythoa caesia. Mar Ecol Prog Ser 234:105–109
Carlos AA, Baillie BK, Kawachi M, Maruyama T (1999) Phylogenetic position of Symbiodinium (Dinophyceae) isolates from Tridacnids (Bvalvia), Cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J Phycol 35:1054–1062
Chen CA, Yang Y-W, Wei NV, Tsai W-S, Fang L-S (2005) Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs 24:11–22
Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34
Cook CB, D’elia CF (1987) Are natural populations of zooxanthellae ever nutrient-limited? Symbiosis 4:199–212
Costa CF, Sassi R, Amaral FD (2004) Population density and photosynthetic pigment content in symbiotic dinoflagellates in the Brazilian scleractinian coral Montastrea cavernosa (linnaeus, 1767). Braz J Oceanogr 52(2):93–99
Costa CF, Sassi R, Gorlach-Lira K (2008) Zooxanthellae genotypes in the coral Siderastrea stellata from coastal reefs in northeastern Brazil. J Exp Mar Biol Ecol 367:149–152
Costa CF, Sassi R, Gorlach-Lira K, Lajeunesse TC, Fitt WK (2013) Seasonal changes in zooxanthellae harbored by zoanthids (Cnidaria, Zoanthidea) from coastal reefs in northeastern Brazil. Pan Am J Aquat Sci 8:253–264
Edmunds PJ, Davies SP (1986) An energy budget for Porites porites (Scleractinia). Mar Biol 92:339–347
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. Mol Ecol 13:2445–2458
Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and bioenergetics of a symbiotic coral. Bioscience 34:705–709
Fay SA, Weber MX, Lipps JH (2009) The distribution of Symbiodinium diversity within individual host foraminifera. Coral Reefs 28:717–726
Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, Lajeunesse TC (2010) The relative significance of host–habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 1:250–263
Furla P, Allemand D, Shick JM, Ferrier-Pagès C, Richier S, Plantivaux A, Merle PL, Tambutté S (2005) The symbiotic anthozoan: a physiological chimera between alga and animal. Integr Comp Biol 45:595–604
Garren M, Walsh SM, Caccone A, Knowlton N (2006) 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 25:503–512
Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17
Hennige SJ, Mcginley MP, Grottoli AG, Warner ME (2011) Photoinhibition of Symbiodinium spp. within the reef corals Montastraea faveolata and Porites astreoides: implications for coral bleaching. Mar Biol 158:2515–2526
Hill M, Allenby A, Ramsby B, Schönberg C, Hill A (2011) Symbiodinium diversity among host clionid sponges from Caribbean and Pacific reefs: evidence of heteroplasmy and putative host-specific symbiont lineages. Mol Phylogenet Evol 59:81–88
Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, Kim HS, Yih W, Yamashita H, LaJeunesse TC (2014) Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium Clade E. J Euk Microbiol 61:75–94
Kamezaki M, Higa M, Hirose M, Suda S, Reimer JD (2013) Different zooxanthellae types in populations of the zoanthid Zoanthus sansibaricus along depth gradients in Okinawa, Japan. Mar Biodivers 43:61–70
Karako-Lampert S, Katcoff DJ, Achituv Y, Dubinsky D, Stambler N (2004) Do clades of symbiotic dinoflagellates in scleractinian corals of the Gulf of Eilat (Red Sea) differ from those of other coral reefs? J Exp Mar Biol Ecol 311:301–314
Kinzie RA, Chee GS (1979) The effect of different zooxanthellae on the growth of experimentally reinfected hosts. Biol Bull 156:315–327
Kinzie RA, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biol Bull 200:51–58
Kirkendale L (2009) Their day in the sun: molecular phylogenetics and origin of photosymbiosis in the “other” group of photosymbiotic marine bivalves (Cardiidae:Fraginae). Biol J Linn Soc 97:448–465
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. J Phycol 880:866–880
LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PloS One e29013
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. Limnol Oceanogr 48:2046–2054
LaJeunesse TC, Bhagooli R, Hidaka M, Done T, Devantier L, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004a) Closely-related Symbiodinium spp. differ in relative dominance within coral reef host communities across environmental, latitudinal, and biogeographic gradients. Mar Ecol Progr Ser 284:147–161
Lajeunesse TC, Thornhill DJ, Cox E, Stanton F, Fitt WK, Schmidt GW (2004b) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603
Lajeunesse TC, Reyes-Bonilla H, Warner ME, Wills M, Schmidt GW, Fitt WK (2008) Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanogr 53:719–727
Lajeunesse TC, Pettay T, Phongsuwan N, Brown B, Obura D, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37:785–800
LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with Cnidaria. J Phycol 48:1380–1391
LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress tolerant endosymbionts in the dinoflagellate genus Symbiodinium Clade D are different species. Phycologia 53:305–319
Loh WKW, Loi T, Carter D, Hoegh-Guldberg O (2006) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Mar Ecol Prog Ser 222:97–107
Magalon H, Flot JF, Baudry E (2007) Molecular identification of symbiotic dinoflagellates in Pacific corals in the genus Pocillopora. Coral Reefs 26:551–558
Moore EJ, Gosliner TM (2011) Molecular phylogeny and evolution of symbiosis in a clade of Indopacific nudibranchs. Mol Phylogenet Evol 58:116–123
Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Coral reefs, 1st edn. Elsevier, Amsterdam, pp 75–87
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient poor environments. Bioscience 27:454–460
Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, Mccloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. P Roy Soc Lond B Bio 236:311–324
Neale PJ, Banaszak AT, Jarriel CR (1998) Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis. J Phycol 34:928–938
Oigman-Pszczol SS, Figueiredo MAO, Creed JC (2004) Distribution of benthic communities on the tropical rocky subtidal of Armacão dos Búzios, Southeastern Brazil. Mar Ecol 25:173–190
Pérez CD, Vila-Nova DA, Santos AM (2005) Associated community with the zoanthid Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiologia 548:207–215
Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 6:1069–1078
Pochon X, Stat M, Takabayashi M, Chasqui L, Chauka LJ, Logan DDK, Gates RD (2010) Comparison of endosymbiotic and free-living Symbiodinium(Dinophyceae) diversity in a Hawaiian reef environment. J Phycol 4:53–65
Pochon X, Putnam HM, Burki F, Gates RD (2012) Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLoS ONE 7:e29816
Rabelo EF, Soares MO, Matthews-Cascon H (2013) Competitive interactions among zoanthids (Cnidaria: Zoanthidae) in an intertidal zone of Northeastern Brazil. Braz J Oceanogr 61:35–42
Rabelo EF, Soares MO, Bezerra LEA, Matthews-Cascon H (2014) Distribution pattern of Zoanthids (Cnidaria: Zoantharia) on a tropical reef. Mar Biol Res (in press)
Reef R, Kaniewska P, Hoegh-Guldberg O (2009) Coral skeletons defend against ultraviolet radiation. PLoS ONE 4:e7995
Reimer AA (1971) Observations on the relationships between several species of tropical zoanthids (Zoanthidea, Coelenterate) and their zooxanthellae. J Exp Mar Boil Ecol 7:207–214
Reimer JD, Hickman CP Jr (2009) Preliminary survey of zooxanthellate Zoanthids (Cnidaria: Hexacorallia) of the Galapagos, and associated symbiotic dinoflagellates (Symbiodinium spp.). Galápagos Res 66:14–19
Reimer JD, Todd PA (2009) Preliminary molecular examination of zooxanthellate zoanthids (Hexacorallia: Zoantharia) and associated zooxanthellae (Symbiodinium spp.) diversity in Singapore. Raffles Bull Zool 22:103–120
Reimer JD, Ono S, Takishita K, Tsukahara J, Maruyama J (2006a) Molecular evidence suggesting species in the Zoanthid genera Palythoa and Protopalythoa (Anthozoa: Hexacorallia) are congeneric. Zool Sci 23:87–94
Reimer JD, Takishita K, Maruyama T (2006b) Molecular identification of symbiotic dinoflagellates (Symbiodinium spp.) from Palythoa spp. (Anthozoa: Hexacorallia) in Japan. Coral Reefs 25:521–527
Reimer JD, Takishita K, Ono S, Maruyama T, Tsukahara J (2006c) Latitudinal and intracolony ITS-rDNA sequence variation in the symbiotic dinoflagellate genus Symbiodinium (Dinophyceae) in Zoanthus sansibaricus (Anthozoa:Hexacorallia). Phycol Res 54:122–132
Reimer JD, Ono S, Tsukahara J, Takishita K, Maruyama T (2007) Non-seasonal clade-specificity and subclade microvariation in symbiotic dinoflagellates (Symbiodinium spp.) in Zoanthus sansibaricus (Anthozoa: Hexacorallia) at Kagoshima Bay, Japan. Phycol Res 55:58–65
Reimer JD, Hirose M, Wirtz P (2010) Zoanthids of the Cape Verde islands and their symbionts: previously unexamined diversity in the Northeastern Atlantic. Contrib Zool 79:147–163
Reimer JD, Hirose M, Yanagi K, Sinniger F (2011) Marine invertebrate diversity in the oceanic Ogasawara Islands: a molecular examination of zoanthids (Anthozoa: Hexacorallia) and their Symbiodinium (Dinophyceae). Syst and Biodivers 9:133–143
Reimer JD, Foord C, Irei Y (2012) Species diversity of shallow water zoanthids (Cnidaria: Anthozoa: Hexacorallia) in Florida. J Mar Biol Article ID 856079, 14 pages
Reimer JD, Irei Y, Fujii T, Yang S (2013) Molecular analyses of shallow-water zooxanthellate zoanthids (Cnidaria: Hexacorallia) from Taiwan and their Symbiodinium spp. Zool Stud 52:1–16
Roger SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant-tissues. Plant Mol Biol 5:69–76
Rowan R, Powers DA (1991a) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351
Rowan R, Powers DA (1991b) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73
Ryland SJ, Lancaster JE (2003) Revision of method for separating species of Protopalythoa (Hexacorallia: Zoanthidea) in the tropical West Pacific. Invertrebr Syst 17:407–428
Sampayo EM, Ridgeway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of S. microadriaticum. Proc R Soc Lond B 207:445–460
Sebens KP (1977) Autotrophic and heterotrophic nutrition of coral reef zoanthids. Proc 3rd Intern Coral Reef Symp 1:398–404
Sebens KP (1982) Intertidal distribuition of zoanthids on the Caribbean coast of Panama: effects of predaction and desiccation. Bull Mar Sci 32:316–335
Singleton DR, Michelle AF, Stephen LRA, William BW (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4374–4376
Smith RT, Pinzón JH, Lajeunesse TC (2009) Symbiodinium (Dinophyta) diversity and stability in aquarium corals. J Phycol 45:1030–1036
Soares MO, Rabelo EF (2014) Primeiro registro de branqueamento de corais no litoral do Ceará (Ne, Brasil): indicador das mudanças climáticas? Geociênc 33:1–10
Suchanek TH, Green DJ (1981) Interespecific competition between Palythoa caribaeorum and other sessile invertebrates on St. Croix Reefs, U.S. Virgin Islands. Proc 4rd Intern Coral Reef Symp 2:679–684
Thornhill DJ, Lord JB (2010) Secondary structure models for the internal transcribed spacer (ITS) region 1 from symbiotic dinoflagellates. Protist 161:434–451
Thornhill DJ, Lajeunesse TC, Santos SR (2007) Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Mol Ecol 16:5326–5340
Thornhill DJ, Lewis AM, Wham DC, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367
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. Biol Bull 201:360–373
Trench RK (1974) Nutritional potentials in Zoanthus sociatus (Coelenterata, Anthozoa). Helgol Mar Res 974:174–216
Trench RK (1993) Microalgal-invertebrate symbioses: a review. Endocytobiosis Cell Res 9:135–175
Trench RK (1997) Diversity of symbiotic dinoflagellates and the evolution of microalgal-invertebrate symbioses. Proc Eighth Int Coral Reef Symp 2:1275–1286
van Oppen MJH, Palstra FP, Piquet AM, Miller DJ (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc Biol Sci 268:1759–1767
van Oppen MJH, Mieog JC, Sánchez CA, Fabricius KE (2005) Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Mol Ecol 14:2403–2417
Villaça R, Pitombo FB (1997) Benthic communities of shallow-water reefs of Abrolhos, Brazil. Rev Bras Oceanogr 45:35–43
Visram S, Douglas AE (2006) Molecular diversity of symbiotic algae (zooxanthellae) in scleractinian corals of Kenya. Coral Reefs 25:172–176
Yamashita H, Suzuki G, Hayashibara T, Koike K (2010) Do corals select zooxanthellae by alternative discharge? Mar Biol 158:87–100
Yellowlees D, Tav R, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694
Acknowledgments
This study was conducted in partnership with researchers from the Laboratory of Microbial Ecology and Biotechnology (Lembiotech), whom we sincerely thank. The authors gratefully acknowledge the collaboration of Dr. Janet Reid for English review and valuable suggestions and MSc. Taffarel Torres for phylogenetic tree suggestions. The study received support from CAPES, through the Project Marine Sciences, process no. 0532/2010.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rabelo, E.F., Rocha, L.L., Colares, G.B. et al. Symbiodinium diversity associated with zoanthids (Cnidaria: Hexacorallia) in Northeastern Brazil. Symbiosis 64, 105–113 (2014). https://doi.org/10.1007/s13199-014-0308-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-014-0308-9