Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals

Microbial Ecology

Volumn 71, Issue 3, 2016, Pages 771-783

  Lee, Moo Joon ^a   Jeong, Hae Jin ^a   Jang, Se Hyeon ^a   Lee, Sung Yeon ^a   Kang, Nam Seon ^a   Lee, Kyung Ha ^a   Kim, Hyung Seop ^b   Wham, Drew C ^c   LaJeunesse, Todd C ^c  

^a Seoul National University   (South Korea)

^b Kunsan National University   (South Korea)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Coral microbiome; Dinoflagellates; Functional ecology; Host symbiont specificity; Quantitative PCR

Indexed keywords

NITROGEN;

ANIMAL; ANTHOZOA; BIODIVERSITY; CLASSIFICATION; DINOFLAGELLATE; ISOLATION AND PURIFICATION; METABOLISM; PARASITOLOGY; PHYLOGENY; PHYSIOLOGY; SEASON; SYMBIOSIS;

ANIMALS; ANTHOZOA; BIODIVERSITY; DINOFLAGELLIDA; NITROGEN; PHYLOGENY; SEASONS; SYMBIOSIS;

EID: 84961135181     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-015-0724-2     Document Type: Article

References (95)

1. McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236. doi:10.1073/pnas.1218525110
2. Knowlton N, Rohwer F (2003) Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am Nat 162:S51–62. doi:10.1086/378684
3. Kirk NL, Thornhill DJ, Kemp DW, Fitt WK, Santos SR (2013) Ubiquitous associations and a peak fall prevalence between apicomplexan symbionts and reef corals in Florida and the Bahamas. Coral Reefs 32:847–858. doi:10.1007/s00338-013-1038-9
4. Amend AS, Barshis DJ, Oliver TA (2012) Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J 6:1291–1301. doi:10.1038/ismej.2011.193
5. 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. doi:10.1098/rspb.2006.3567
6. 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. doi:10.1038/40843
7. Jones AM, Berkelmans R, van Oppen MJ, 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. Proc Biol Sci 275:1359–1365. doi:10.1098/rspb.2008.0069
8. LaJeunesse TC, Smith RT, Finney J, Oxenford H (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proc Biol Sci 276:4139–4148. doi:10.1098/rspb.2009.1405
9. Kemp DW, Hernandez-Pech X, Iglesias-Prieto R, Fitt WK, Schmidt GW (2014) Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol Oceanogr 59:788–797. doi:10.4319/lo.2014.59.3.0788
10. McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7. doi:10.3354/meps09914
11. Stat M, Loh WKW, LaJeunesse TC, Hoegh-Guldberg O, Carter DA (2009) Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709–713. doi:10.1007/s00338-009-0509-5
12. Goulet TL, LaJeunesse TC, Fabricius KE (2008) Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event. Mar Biol 154:795–804. doi:10.1007/s00227-008-0972-5
13. 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. doi:10.1007/s00338-007-0244-8
14. Silverstein RN, Correa AM, Baker AC (2012) Specificity is rarely absolute in coral-algal symbiosis: implications for coral response to climate change. Proc Biol Sci 279:2609–2618. doi:10.1098/rspb.2012.0055
15. Kennedy EV, Foster NL, Mumby PJ, Stevens JR (2015) Widespread prevalence of cryptic Symbiodinium D in the key Caribbean reef builder, Orbicella annularis. Coral Reefs 34:519–531. doi:10.1007/s00338-015-1264-4
16. Thomas L, Kendrick GA, Kennington WJ, Richards ZT, Stat M (2014) Exploring Symbiodinium diversity and host specificity in Acropora corals from geographical extremes of Western Australia with 454 amplicon pyrosequencing. Mol Ecol 23:3113–3126. doi:10.1111/mec.12801
17. Quigley KM, Davies SW, Kenkel CD, Willis BL, Matz MV, Bay LK (2014) Deep-sequencing method for quantifying background abundances of symbiodinium types: exploring the rare symbiodinium biosphere in reef-building corals. PLoS One 9:e94297. doi:10.1371/journal.pone.0094297
18. Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barbrook A, Howe CJ, LaJeunesse TC, Voolstra CR (2014) Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol Ecol 23:4418–4433
19. 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 60:250–263. doi:10.1007/s00248-010-9681-y
20. Ulstrup KE, Van Oppen MJH (2003) Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484. doi:10.1046/j.1365-294X.2003.01988.x
21. LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161. doi:10.3354/meps284147
22. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, 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. doi:10.1111/j.1365-2699.2010.02273.x
23. Tonk L, Sampayo EM, LaJeunesse TC, Schrameyer V, Hoegh-Guldberg O (2014) Symbiodinium (Dinophyceae) diversity in reef-invertebrates along an offshore to inshore reef gradient near Lizard Island, Great Barrier Reef. J Phycol 50:552–563. doi:10.1111/jpy.12185
24. LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53:305–319. doi:10.2216/13-186.1
25. Baker AC, Romanski AM (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: comment on Goulet (2006). Mar Ecol Prog Ser 335:237–242. doi:10.3354/meps335237
26. Santos SR, Taylor DJ, Coffroth MA (2001) Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: implications for extrapolating to the intact symbiosis. J Phycol 37:900–912. doi:10.1046/j.1529-8817.2001.00194.x
27. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400. doi:10.1007/s00227-002-0829-2
28. 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 Eukaryot Microbiol 61:75–94. doi:10.1111/jeu.12088
29. LaJeunesse TC, Lee SY, Gil-Agudelo DL, Knowlton N, Jeong HJ (2015) Symbiodinium necroappetens sp nov (Dinophyceae): an opportunist 'zooxanthella' found in bleached and diseased tissues of Caribbean reef corals. Eur J Phycol 50:223–238. doi:10.1080/09670262.2015.1025857
30. Parkinson JE, Coffroth MA, LaJeunesse TC (2015) New species of Clade B Symbiodinium (Dinophyceae) from the greater Caribbean belong to different functional guilds: S. aenigmaticum sp. nov., S. antillogorgium sp. nov., S. endomadracis sp. nov., and S. pseudominutum sp. nov. J Phycol 51:850–858. doi:10.1111/jpy.12340
31. 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 37:866–880. doi:10.1046/j.1529-8817.2001.01031.x
32. Song JI (1991) A systematic study on the Korean Anthozoa. 12. Order Scleractinia. Korean J Syst Zool 7:127–150
33. Denis V, Chen CA, Song JI, Woo S (2013) Alveopora japonica beds thriving under kelp. Coral Reefs 32:503–503. doi:10.1007/s00338-013-1019-z
34. Sugihara K, Yamano H, Choi K-S, Hyeong K (2014) Zooxanthellate scleractinian corals of Jeju Island, Republic of Korea: 111-130. doi: 10.1007/978-4-431-54783-9_6
35. Sheppard A, Fenner D, Edwards A, Abrar M, Ochavillo D (2008) Alveopora japonica. The IUCN Red List of Threatened Species 2008
36. Rodriguez-Lanetty M, Chang S-J, Song J-I (2003) Specificity of two temperate dinoflagellate-anthozoan associations from the north-western Pacific Ocean. Mar Biol 143:1193–1199. doi:10.1007/s00227-003-1165-x
37. Chang S-J, Rodriguez-Lanetty M, Yanagi K, Nojima S, Song J-I (2011) Two anthozoans, Entacmaea quadricolor(order Actiniaria) and Alveopora japonica(order Scleractinia), host consistent genotypes of Symbiodinium spp. across geographic ranges in the northwestern Pacific Ocean. Anim Cells Syst 15:315–324. doi:10.1080/19768354.2011.611174
38. De Palmas S, Denis V, Ribas-Deulofeu L, Loubeyres M, Woo S, Hwang SJ, Song JI, Chen CA (2015) Symbiodinium spp. associated with high-latitude scleractinian corals from Jeju Island, South Korea. Coral Reefs 34:919–925. doi:10.1007/s00338-015-1286-y
39. Lien YT, Fukami H, Yamashita Y (2012) Symbiodinium clade C dominates zooxanthellate corals (Scleractinia) in the temperate region of Japan. Zool Sci 29:173–180. doi:10.2108/zsj.29.173
40. APHA (1995) American Public Health Association. Standard methods for the examination of water and wastewater. APHA, Washington D. C
41. Litaker RW, Vandersea MW, Kibler SR, Reece KS, Stokes NA, Steidinger KA, Millie DF, Bendis J, Pigg RJ, Tester PA (2003) Identification of Pfiesteria piscicida(Dinophyceae) and Pfiesteria-like organisms using internal transcribed spacer-specific PCR assays. J Phycol 39:754–761
42. Kang NS, Jeong HJ, Moestrup O, Park TG (2011) Gyrodiniellum shiwhaense n. gen., n. sp., a new planktonic heterotrophic dinoflagellate from the coastal waters of western Korea: morphology and ribosomal DNA gene sequence. J Eukaryot Microbiol 58:284–309. doi:10.1111/j.1550-7408.2011.00544.x
43. Swofford DL (2014) PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, Massachusetts
44. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi: 10.1093/bioinformatics/btg180
45. 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. doi:10.4319/lo.2008.53.2.0719
46. Team R-C (2015) R: a language and environment for statistical computing. https://www.R-project.org
47. Conover WJ (1999) Practical nonparametric statistics. Wiley, New York
48. Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River
49. 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 139:1069–1078. doi: 10.1007/s002270100674
50. Pochon X, Garcia-Cuetos L, Baker AC, Castella E, Pawlowski J (2007) One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 26:867–882. doi: 10.1007/s00338-007-0279-x
51. Garcia-Cuetos L, Pochon X, Pawlowski J (2005) Molecular evidence for host–symbiont specificity in soritid foraminifera. Protist 156:399–412. doi: 10.1016/j.protis.2005.08.003
52. Muscatine L (1973) Nutrition of corals Biology and Geology of Coral Reefs, pp. 77-115
53. Smayda TJ (2002) Adaptive ecology, growth strategies and the global bloom expansion of dinoflagellates. J Oceanogr 58:281–294. doi:10.1023/A:1015861725470
54. Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Guldberg O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Mar Biol 138:1175–1181. doi:10.1007/s002270100536
55. Silverstein RN, Correa AMS, LaJeunesse TC, Baker AC (2011) Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar Ecol Prog Ser 422:63–75
56. Thornhill DJ, Xiang Y, Pettay DT, Zhong M, Santos SR (2013) Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 22:4499–4515. doi:10.1111/mec.12416
57. 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. doi:10.1111/j.1529-8817.2012.01217.x
58. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinski Z (ed) Coral reefs: ecosystems of the world. Elsevier, New York, pp 75–87
59. Stimson J, Kinzie RA III (1991) The temporal pattern and rate of release of zooxanthellae. J Exp Mar Biol Ecol 153:63–74. doi:10.1016/S0022-0981(05)80006-1
60. Hoegh-Guldberg O, McCloskey LR, Muscatine L (1987) Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea. Coral Reefs 5:201–204. doi:10.1007/BF00300964
61. Jones RJ, Yellowlees D (1997) Regulation and control of intracellular algae (= zooxanthellae) in hard corals. Philos Trans R Soc B Biol Sci 352:457–468. doi:10.1098/rstb.1997.0033
62. Baghdasarian G, Muscatine L (2000) Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biol Bull (Woods Hole) 199:278–286
63. Goulet TL, Coffroth MA (2003) Stability of an octocoral-algal symbiosis over time and space. Mar Ecol Prog Ser 250:117–124
64. 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. Mar Biol 148:711–722. doi:10.1007/s00227-005-0114-2
65. Thornhill DJ, Xiang Y, Fitt WK, Santos SR (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS One 4:e6262. doi:10.1371/journal.pone.0006262
66. Suwa R, Hirose M, Hidaka M (2008) Seasonal fluctuation in zooxanthellar genotype composition and photophysiology in the corals Pavona divaricata and P. decussata. Mar Ecol Prog Ser 361:129–137. doi:10.3354/meps07372
67. Pettay DT, Wham DC, Pinzón JH, LaJeunesse TC (2011) Genotypic diversity and spatial-temporal distribution of Symbiodinium clones in an abundant reef coral. Mol Ecol 20:5197–5212. doi:10.1111/j.1365-294X.2011.05357.x
68. Baums IB, Devlin-Durante MK, LaJeunesse TC (2014) New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies. Mol Ecol 23:4203–4215. doi:10.1111/mec.12788
69. Thornhill DJ, Fitt WK, Schmidt GW (2006) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515–519. doi:10.1007/s00338-006-0157-y
70. LaJeunesse TC (2005) "Species" radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581. doi:10.1093/molbev/msi042
71. Harii S, Omori M, Yamakawa H, Koike Y (2001) Sexual reproduction and larval settlement of the zooxanthellate coral Alveopora japonica Eguchi at high latitudes. Coral Reefs 20:19–23. doi:10.1007/s003380000134
72. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685
73. Hsu C-M, Keshavmurthy S, Denis V, Kuo C-Y, Wang J-T, Meng P-J, Chen CA (2012) Temporal and spatial variations in symbiont communities of catch bowl coral Isopora palifera (Scleractinia: Acroporidae) on reefs in Kenting National Park, Taiwan. Zool Stud 51:1343–1353
74. Sachs JL, Simms EL (2006) Pathways to mutualism breakdown. Trends Ecol Evol 21:585–592. doi:10.1016/j.tree.2006.06.018
75. Douglas AE (2008) Conflict, cheats and the persistence of symbioses. New Phytol 177:849–858. doi:10.1111/j.1469-8137.2007.02326.x
76. 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 Symbiodinium microadriaticum. Proc R Soc Lond, Ser B: Biol Sci 207. doi:10.1098/rspb.1980.0031
77. Eloe-Fadrosh EA, Rasko DA (2013) The human microbiome: from symbiosis to pathogenesis. Annu Rev Med 64:145–163. doi:10.1146/annurev-med-010312-133513
78. Houlbreque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev Camb Philos Soc 84:1–17. doi:10.1111/j.1469-185X.2008.00058.x
79. Hall NM, Berry KLE, Rintoul L, Hoogenboom MO (2015) Microplastic ingestion by scleractinian corals. Mar Biol 162:725–732. doi:10.1007/s00227-015-2619-7
80. Leal MC, Ferrier-Pages C, Calado R, Thompson ME, Frischer ME, Nejstgaard JC (2013) Coral feeding on microalgae assessed with molecular trophic markers. Mol Ecol 23:3870–3876. doi:10.1111/mec.12486
81. Toller W, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the caribbean corals Montastrea annularis and M. faveolata following experimental and disease-associated bleaching. Biol Bull 2001:360–373
82. Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20:3823–3833. doi:10.1111/gcb.12658
83. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689. doi:10.1146/annurev.ecolsys.34.011802.132417
84. Smith RT (2008) Specificity, stability and comparative physiology of coral-Symbiodinium mutualisms: evaluating the potential for acclimation and/or adaptation in reef corals. Florida International University
85. Pettay DT, Wham DC, Smith RT, Iglesias-Prieto R, LaJeunesse TC (2015) Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci U S A 112:7513–7518. doi:10.1073/pnas.1502283112
86. LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magana AL, Perez AL, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc Biol Sci 277:2925–2934. doi:10.1098/rspb.2010.0385
87. Hirose M, Reimer JD, Hidaka M, Suda S (2008) Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar Biol 155:105–112. doi:10.1007/s00227-008-1011-2
88. Porto I, Granados C, Restrepo JC, Sanchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS One 3:e2160. doi:10.1371/journal.pone.0002160
89. Littman RA, van Oppen MJH, Willis BL (2008) Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J Exp Mar Biol Ecol 364:48–53. doi:10.1016/j.jembe.2008.06.034
90. Takabayashi M, Adams LM, Pochon X, Gates RD (2011) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai'i and Florida. Coral Reefs 31:157–167. doi:10.1007/s00338-011-0832-5
91. Sweet MJ (2013) Symbiodinium diversity within Acropora muricata and the surrounding environment. Mar Ecol 35:343–353. doi:10.1111/maec.12092
92. Kohli GS, Neilan BA, Brown MV, Hoppenrath M, Murray SA (2014) Cob gene pyrosequencing enables characterization of benthic dinoflagellate diversity and biogeography. Environ Microbiol 16:467–485. doi:10.1111/1462-2920.12275
93. Jeong HJ, Yoo YD, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin W, Nam SW (2012) Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc Nat Acad Sci 109:12604–12609. doi: 10.1073/pnas.1204302109
94. LaJeunesse TC, Loh W, Trench RK (2009) Do introduced endosymbiotic dinoflagellates ‘take’ to new hosts? Biol Invasions 11:995–1003. doi:10.1007/s10530-008-9311-5
95. Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, Lajeunesse TC (2015) Symbiodinium tridacnidorum sp nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank. Eur J Phycol 50:155–172 doi:10.1080/09670262.2015.1018336