Unlocking the phylogenetic diversity, primary habitats, and abundances of free-living Symbiodiniaceae on a coral reef.
ITS2
Symbiodiniaceae
benthic
epiphytic
free-living
habitat
qPCR
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
14
09
2019
revised:
21
10
2020
accepted:
27
10
2020
pubmed:
4
11
2020
medline:
22
6
2021
entrez:
3
11
2020
Statut:
ppublish
Résumé
Dinoflagellates of the family Symbiodiniaceae form mutualistic symbioses with marine invertebrates such as reef-building corals, but also inhabit reef environments as free-living cells. Most coral species acquire Symbiodiniaceae horizontally from the surrounding environment during the larval and/or recruitment phase, however the phylogenetic diversity and ecology of free-living Symbiodiniaceae on coral reefs is largely unknown. We coupled environmental DNA sequencing and genus-specific qPCR to resolve the community structure and cell abundances of free-living Symbiodiniaceae in the water column, sediment, and macroalgae and compared these to coral symbionts. Sampling was conducted at two time points, one of which coincided with the annual coral spawning event when recombination between hosts and free-living Symbiodiniaceae is assumed to be critical. Amplicons of the internal transcribed spacer (ITS2) region were assigned to 12 of the 15 Symbiodiniaceae genera or genera-equivalent lineages. Community compositions were separated by habitat, with water samples containing a high proportion of sequences corresponding to coral symbionts of the genus Cladocopium, potentially as a result of cell expulsion from in hospite populations. Sediment-associated Symbiodiniaceae communities were distinct, potentially due to the presence of exclusively free-living species. Intriguingly, macroalgal surfaces displayed the highest cell abundances of Symbiodiniaceae, suggesting a key role for macroalgae in ensuring the ecological success of corals through maintenance of a continuum between environmental and symbiotic populations of Symbiodiniaceae.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
343-360Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Abrego, D., Van Oppen, M. J., & Willis, B. L. (2009). Highly infectious symbiont dominates initial uptake in coral juveniles. Molecular Ecology, 18(16), 3518-3531. https://doi.org/10.1111/j.1365-294X.2009.04275.x
Adams, L. M., Cumbo, V. R., & Takabayashi, M. (2009). Exposure to sediment enhances primary acquisition of Symbiodinium by asymbiotic coral larvae. Marine Ecology Progress Series, 377, 149-156. https://doi.org/10.3354/meps07834
Ali, A., Kriefall, N. G., Emery, L. E., Kenkel, C. D., Matz, M. V., & Davies, S. W. (2019). Recruit symbiosis establishment and Symbiodiniaceae composition influenced by adult corals and reef sediment. Coral Reefs, 38(3), 405-415. https://doi.org/10.1007/s00338-019-01790-z
Aligizaki, K., & Nikolaidis, G. (2006). The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the North Aegean Sea. Greece. Harmful Algae, 5(6), 717-730. https://doi.org/10.1016/j.hal.2006.02.005
Ankenbrand, M. J., Keller, A., Wolf, M., Schultz, J., & Förster, F. (2015). ITS2 database V: Twice as much. Molecular Biology and Evolution, 32(11), 3030-3032.
Baird, A. H., Cumbo, V. R., Leggat, W., & Rodriguez-Lanetty, M. (2007). Fidelity and flexibility in coral symbioses. Marine Ecology Progress Series, 347, 307-309. https://doi.org/10.3354/meps07220
Baird, A. H., Guest, J. R., & Willis, B. L. (2009). Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annual Review of Ecology, Evolution, and Systematics, 40, 551-571. https://doi.org/10.1146/annurev.ecolsys.110308.120220
Berkelmans, R., & Van Oppen, M. J. (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 the Royal Society B: Biological Sciences, 273(1599), 2305-2312.
Boulotte, N. M., Dalton, S. J., Carroll, A. G., Harrison, P. L., Putnam, H. M., Peplow, L. M., & van Oppen, M. J. (2016). Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. The ISME Journal, 10(11), 2693. https://doi.org/10.1038/ismej.2016.54
Byler, K. A., Carmi-Veal, M., Fine, M., & Goulet, T. L. (2013). Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS One, 8(3), e59596. https://doi.org/10.1371/journal.pone.0059596
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581. https://doi.org/10.1038/nmeth.3869
Camp, E. F., Suggett, D. J., Pogoreutz, C., Nitschke, M. R., Houlbreque, F., Hume, B. C., Gardner, S., Zampighi, M., Rodolfo-Metalpa, R., & Voolstra, C. R. (2020). Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment. Coral Reefs, 39, 1-16. https://doi.org/10.1007/s00338-019-01889-3
Carlos, A. A., Baillie, B. K., Kawachi, M., & Maruyama, T. (1999). Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. Journal of Phycology, 35(5), 1054-1062. https://doi.org/10.1046/j.1529-8817.1999.3551054.x
Castro-Sanguino, C., & Sánchez, J. A. (2011). Dispersal of Symbiodinium by the stoplight parrotfish Sparisoma viride. Biology Letters, 8(2), 282-286.
Ceccarelli, D. M., Loffler, Z., Bourne, D. G., Al Moajil-Cole, G. S., Boström-Einarsson, L., Evans-Illidge, E., Fabricius, K., Glasl, B., Marshall, P., McLeod, I., Read, M., Schaffelke, B., Smith, A. K., Jorda, G. T., Williamson, D. H., & Bay, L. (2018). Rehabilitation of coral reefs through removal of macroalgae: State of knowledge and considerations for management and implementation. Restoration Ecology, 26(5), 827-838. https://doi.org/10.1111/rec.12852
Charif, D., & Lobry, J. R. (2007). SeqinR 1.0-2: A contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. In U. Bastolla, M. Porto, H. E. Roman, & M. Vendruscolo (Eds.), Structural Approaches to Sequence Evolution (pp. 207-232). Springer.
Claar, D. C., Tietjen, K. L., Cox, K. D., Gates, R. D., & Baum, J. K. (2020). Chronic disturbance modulates symbiont (Symbiodiniaceae) beta diversity on a coral reef. Scientific Reports, 10(1), 1-13. https://doi.org/10.1038/s41598-020-60929-z
Coffroth, M. A., Lewis, C. F., Santos, S. R., & Weaver, J. L. (2006). Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Current Biology, 16(23), R985-R987. https://doi.org/10.1016/j.cub.2006.10.049
Coffroth, M. A., & Santos, S. R. (2005). Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist, 156, 19-34. https://doi.org/10.1016/j.protis.2005.02.004
Coffroth, M. A., Santos, S. R., & Goulet, T. L. (2001). Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Marine Ecology Progress Series, 222, 85-96. https://doi.org/10.3354/meps222085
Cumbo, V., Baird, A., & Van Oppen, M. (2013). The promiscuous larvae: Flexibility in the establishment of symbiosis in corals. Coral Reefs, 32(1), 111-120. https://doi.org/10.1007/s00338-012-0951-7
Cunning, R., Yost, D. M., Guarinello, M. L., Putnam, H. M., & Gates, R. D. (2015). Variability of Symbiodinium communities in waters, sediments, and corals of thermally distinct reef pools in American Samoa. PLoS One, 10(12), e0145099. https://doi.org/10.1371/journal.pone.0145099
Fisher, P., Malme, M., & Dove, S. (2012). The effect of temperature stress on coral-Symbiodinium associations containing distinct symbiont types. Coral Reefs, 31(2), 473-485. https://doi.org/10.1007/s00338-011-0853-0
Fujise, L., Nitschke, M. R., Frommlet, J. C., Serôdio, J., Woodcock, S., Ralph, P. J., & Suggett, D. J. (2018). Cell cycle dynamics of cultured coral endosymbiotic microalgae (Symbiodinium) across different types (species) under alternate light and temperature conditions. Journal of Eukaryotic Microbiology, 65(4), 505-517.
Gardner, S. G., Camp, E. F., Smith, D. J., Kahlke, T., Osman, E. O., Gendron, G., Hume, B. C. C., Pogoreutz, C., Voolstra, C. R., & Suggett, D. J. (2019). Coral microbiome diversity reflects mass coral bleaching susceptibility during the 2016 El Niño heat wave. Ecology and Evolution, 9(3), 938-956. https://doi.org/10.1002/ece3.4662
Gardner, S. G., Raina, J.-B., Nitschke, M. R., Nielsen, D. A., Stat, M., Motti, C. A., Ralph, P. J., & Petrou, K. (2017). A multi-trait systems approach reveals a response cascade to bleaching in corals. BMC Biology, 15(1), 117. https://doi.org/10.1186/s12915-017-0459-2
Gissi, F., Stauber, J., Reichelt-Brushett, A., Harrison, P. L., & Jolley, D. F. (2017). Inhibition in fertilisation of coral gametes following exposure to nickel and copper. Ecotoxicology and Environmental Safety, 145, 32-41. https://doi.org/10.1016/j.ecoenv.2017.07.009
Gómez-Cabrera, M. C., Ortiz, J., Loh, W., Ward, S., & Hoegh-Guldberg, O. (2008). Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs, 27(1), 219-226. https://doi.org/10.1007/s00338-007-0315-x
Granados-Cifuentes, C., Neigel, J., Leberg, P., & Rodriguez-Lanetty, M. (2015). Genetic diversity of free-living Symbiodinium in the Caribbean: The importance of habitats and seasons. Coral Reefs, 34(3), 927-939. https://doi.org/10.1007/s00338-015-1291-1
Grottoli, A. G., Warner, M. E., Levas, S. J., Aschaffenburg, M. D., Schoepf, V., McGinley, M., Baumann, J., & Matsui, Y. (2014). The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Global Change Biology, 20(12), 3823-3833. https://doi.org/10.1111/gcb.12658
Harrison, P. L. (2011). Sexual reproduction of scleractinian corals. In Z. Dubinsky & N. Stambler (Eds.), Coral Reefs: An Ecosystem in Transition (pp. 59-85). Springer.
Hillyer, K. E., Tumanov, S., Villas-Bôas, S., & Davy, S. K. (2016). Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis. Journal of Experimental Biology, 219(4), 516-527. https://doi.org/10.1242/jeb.128660
Hirose, M., Reimer, J. D., Hidaka, M., & Suda, S. (2008). Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Marine Biology, 155(1), 105-112.
Hofmann, L. C., Fink, A., Bischof, K., & de Beer, D. (2015). Microsensor studies on Padina from a natural CO2 seep: Implications of morphology on acclimation to low pH. Journal of Phycology, 51(6), 1106-1115.
Howells, E., Beltran, V., Larsen, N., Bay, L., Willis, B., & Van Oppen, M. (2012). Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change, 2(2), 116. https://doi.org/10.1038/nclimate1330
Hume, B. C., D'Angelo, C., Smith, E. G., Stevens, J. R., Burt, J., & Wiedenmann, J. (2015). Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf. Scientific Reports, 5(1), 1-8.
Hume, B. C., Mejia-Restrepo, A., Voolstra, C. R., & Berumen, M. L. (2020). Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs, 1-19. https://doi.org/10.1007/s00338-020-01917-7
Hume, B. C., Smith, E. G., Ziegler, M., Warrington, H. J., Burt, J. A., LaJeunesse, T. C., Wiedenmann, J., & Voolstra, C. R. (2019). SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Molecular Ecology Resources, 19(4), 1063-1080.
Hume, B. C., Ziegler, M., Poulain, J., Pochon, X., Romac, S., Boissin, E., de Vargas, C., Planes, S., Wincker, P., & Voolstra, C. R. (2018). An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ, 6, e4816.
Jeong, H. J., Lee, S. Y., Kang, N. S., Yoo, Y. D., Lim, A. S., Lee, M. J., Kim, H. S., Yih, W., Yamashita, H., & LaJeunesse, T. (2014). Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium clade E. Journal of Eukaryotic Microbiology, 61(1), 75-94.
Jones, A., Berkelmans, R., van Oppen, M. J., Mieog, J., & 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(1641), 1359-1365.
Kim, H. S., Yih, W., Kim, J. H., Myung, G., & Jeong, H. J. (2011). Abundance of epiphytic dinoflagellates from coastal waters off Jeju Island, Korea During Autumn 2009. Ocean Science Journal, 46(3), 205.
Kohli, G. S., Neilan, B. A., Brown, M. V., Hoppenrath, M., & Murray, S. A. (2014). Cob gene pyrosequencing enables characterization of benthic dinoflagellate diversity and biogeography. Environmental Microbiology, 16(2), 467-485.
Krueger, T., & Gates, R. D. (2012). Cultivating endosymbionts-Host environmental mimics support the survival of Symbiodinium C15 ex hospite. Journal of Experimental Marine Biology and Ecology, 413, 169-176.
LaJeunesse, T. (2002). Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology, 141(2), 387-400.
LaJeunesse, T. (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.
Lajeunesse, T., Bhagooli, R., Hidaka, M., DeVantier, L., Done, T., Schmidt, G., Fitt, W. K., & Hoegh-Guldberg, O. (2004). 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.
LaJeunesse, T., Loh, W., & Trench, R. K. (2009). Do introduced endosymbiotic dinoflagellates ‘take’ to new hosts? Biological Invasions, 11(4), 995-1003.
LaJeunesse, T., Loh, W. K., Van Woesik, R., Hoegh-Guldberg, O., Schmidt, G. W., & Fitt, W. K. (2003). Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnology and Oceanography, 48(5), 2046-2054.
LaJeunesse, T., Parkinson, J. E., Gabrielson, P. W., Jeong, H. J., Reimer, J. D., Voolstra, C. R., & Santos, S. R. (2018). Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology, 28(16), 2570-2580. e2576.
LaJeunesse, T., Smith, R. T., Finney, J., & Oxenford, H. (2009). Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proceedings of the Royal Society B: Biological Sciences, 276(1676), 4139-4148.
LaJeunesse, T., Wham, D. C., Pettay, D. T., Parkinson, J. E., Keshavmurthy, S., & Chen, C. A. (2014). Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia, 53(4), 305-319.
Lee, M. J., Jeong, H. J., Jang, S. H., Lee, S. Y., Kang, N. S., Lee, K. H., Kim, H. S., Wham, D. C., & LaJeunesse, T. C. (2016). Most low-abundance “background” Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microbial Ecology, 71(3), 771-783.
Lee, S. Y., Jeong, H. J., & Lajeunesse, T. (2020). Cladocopium infistulum sp. nov. (Dinophyceae), a thermally tolerant dinoflagellate symbiotic with giant clams from the western Pacific Ocean. Phycologia, 1-12. https://doi.org/10.1080/00318884.2020.1807741 [Epub ahead of print].
Lin, Z., Chen, M., & Chen, J. (2017). Development of a protocol for specific detection and quantification of free-living and endosymbiotic Symbiodinium communities in coral reefs. Aquatic Microbial Ecology, 80(1), 1-13. https://doi.org/10.3354/ame01833
Littman, R. A., van Oppen, M. J., & Willis, B. L. (2008). Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). Journal of Experimental Marine Biology and Ecology, 364(1), 48-53. https://doi.org/10.1016/j.jembe.2008.06.034
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550. https://doi.org/10.1186/s13059-014-0550-8
Lozupone, C., & Knight, R. (2005). UniFrac: A new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology, 71(12), 8228-8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
Madin, J. S., Anderson, K. D., Andreasen, M. H., Bridge, T. C. L., Cairns, S. D., Connolly, S. R., Darling, E. S., Diaz, M., Falster, D. S., Franklin, E. C., Gates, R. D., Harmer, A. M. T., Hoogenboom, M. O., Huang, D., Keith, S. A., Kosnik, M. A., Kuo, C.-Y., Lough, J. M., Lovelock, C. E., … Baird, A. H. (2016). The Coral Trait Database, a curated database of trait information for coral species from the global oceans. Scientific Data, 3, 160017. https://doi.org/10.1038/sdata.2016.17
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet.Journal, 17(1), 10-12. https://doi.org/10.14806/ej.17.1.200
Matthews, J. L., Crowder, C. M., Oakley, C. A., Lutz, A., Roessner, U., Meyer, E., Grossman, A. R., Weis, V. M., & Davy, S. K. (2017). Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. Proceedings of the National Academy of Sciences USA, 114(50), 13194-13199. https://doi.org/10.1073/pnas.1710733114
McCook, L., Jompa, J., & Diaz-Pulido, G. (2001). Competition between corals and algae on coral reefs: A review of evidence and mechanisms. Coral Reefs, 19(4), 400-417. https://doi.org/10.1007/s003380000129
McMurdie, P. J., & Holmes, S. (2013). phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8(4), e61217. https://doi.org/10.1371/journal.pone.0061217
Mercado, J. M., Gordillo, F. J. L., Figueroa, F. L., & Niell, F. X. (1998). External carbonic anhydrase and affinity for inorganic carbon in intertidal macroalgae. Journal of Experimental Marine Biology and Ecology, 221(2), 209-220. https://doi.org/10.1016/S0022-0981(97)00127-5
Moore, R. B. (2006). Molecular ecology and phylogeny of protistan algal symbionts from corals. PhD Thesis, University of Sydney, Sydney, Australia. https://ses.library.usyd.edu.au/handle/2123/1914
Nitschke, M. R., Craveiro, S. C., Brandão, C., Fidalgo, C., Serôdio, J., Calado, A. J., & Frommlet, J. C. (2020). Description of Freudenthalidium gen. nov. and Halluxium gen. nov. to Formally Recognize Clades Fr3 and H as Genera in the Family Symbiodiniaceae (Dinophyceae). Journal of Phycology. https://doi.org/10.1111/jpy.12999 [Epub ahead of print].
Nitschke, M. R., Davy, S., Cribb, T., & Ward, S. (2015). The effect of elevated temperature and substrate on free-living Symbiodinium cultures. Coral Reefs, 34(1), 161-171. https://doi.org/10.1007/s00338-014-1220-8
Nitschke, M. R., Davy, S. K., & Ward, S. (2016). Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment. Coral Reefs, 35(1), 335-344. https://doi.org/10.1007/s00338-015-1349-0
Nitschke, M. R., Gardner, S. G., Goyen, S., Fujise, L., Camp, E. F., Ralph, P. J., & Suggett, D. J. (2018). Utility of photochemical traits as diagnostics of thermal tolerance amongst great barrier reef corals. Frontiers in Marine Science, 5, 45. https://doi.org/10.3389/fmars.2018.00045
Noisette, F., & Hurd, C. (2018). Abiotic and biotic interactions in the diffusive boundary layer of kelp blades create a potential refuge from ocean acidification. Functional Ecology, 32(5), 1329-1342. https://doi.org/10.1111/1365-2435.13067
Oksanen, J., Kindt, R., Legendre, P., O'Hara, B., Stevens, M. H. H., Oksanen, M. J., & Suggests, M. (2007). The vegan package. Community Ecology Package, 10, 631-637.
Parsons, M. L., & Preskitt, L. B. (2007). A survey of epiphytic dinoflagellates from the coastal waters of the island of Hawai 'i. Harmful Algae, 6(5), 658-669. https://doi.org/10.1016/j.hal.2007.01.001
Pettay, D. T., & LaJeunesse, T. C. (2013). Long-range dispersal and high-latitude environments influence the population structure of a “stress-tolerant” dinoflagellate endosymbiont. PLoS One, 8(11), e79208. https://doi.org/10.1371/journal.pone.0079208
Pochon, X., Montoya-Burgos, J. I., Stadelmann, B., & Pawlowski, J. (2006). Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Molecular Phylogenetics and Evolution, 38(1), 20-30. https://doi.org/10.1016/j.ympev.2005.04.028
Pochon, X., Pawlowski, J., Zaninetti, L., & Rowan, R. (2001). High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Marine Biology, 139(6), 1069-1078. https://doi.org/10.1007/s002270100674
Porto, I., Granados, C., Restrepo, J. C., & Sanchez, J. A. (2008). Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean reefs. PLoS One, 3(5), e2160. https://doi.org/10.1371/journal.pone.0002160
Quigley, K. M., Bay, L. K., & Willis, B. L. (2017). Temperature and water quality-related patterns in sediment-associated Symbiodinium communities impact symbiont uptake and fitness of juveniles in the genus Acropora. Frontiers in Marine Science, 4, 401. https://doi.org/10.3389/fmars.2017.00401
Quigley, K. M., Warner, P. A., Bay, L. K., & Willis, B. L. (2018). Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral. Heredity, 121(6), 524-536. https://doi.org/10.1038/s41437-018-0059-0
Ramsby, B. D., Hill, M. S., Thornhill, D. J., Steenhuizen, S. F., Achlatis, M., Lewis, A. M., & LaJeunesse, T. (2017). Sibling species of mutualistic Symbiodinium clade G from bioeroding sponges in the western Pacific and western Atlantic oceans. Journal of Phycology, 53(5), 951-960.
Rowan, R., & Powers, D. A. (1991). Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Marine Ecology Progress Series. Oldendorf, 71(1), 65-73. https://doi.org/10.3354/meps071065
Saad, O. S., Lin, X., Ng, T. Y., Li, L., Ang, P., & Lin, S. (2020). Genome size, rDNA copy, and qPCR assays for Symbiodiniaceae. Frontiers in Microbiology, 11, 847. https://doi.org/10.3389/fmicb.2020.00847
Sampayo, E., Dove, S., & LaJeunesse, T. (2009). Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Molecular Ecology, 18(3), 500-519.
Sampayo, E., Franceschinis, L., Hoegh-Guldberg, O., & Dove, S. (2007). Niche partitioning of closely related symbiotic dinoflagellates. Molecular Ecology, 16(17), 3721-3733. https://doi.org/10.1111/j.1365-294X.2007.03403.x
Santos, S. R., Taylor, D. J., & Coffroth, M. A. (2001). Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. Journal of Phycology, 37(5), 900-912. https://doi.org/10.1046/j.1529-8817.2001.00194.x
Schaffelke, B. (1999). Particulate organic matter as an alternative nutrient source for tropical Sargassum species (Fucales, Phaeophyceae). Journal of Phycology, 35(6), 1150-1157. https://doi.org/10.1046/j.1529-8817.1999.3561150.x
Schliep, K. P. (2011). phangorn: Phylogenetic analysis in R. Bioinformatics, 27(4), 592-593. https://doi.org/10.1093/bioinformatics/btq706
Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., & Weber, C. F. (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23), 7537-7541. https://doi.org/10.1128/AEM.01541-09
Schwarz, J. A., Krupp, D. A., & Weis, V. M. (1999). Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. The Biological Bulletin, 196(1), 70-79. https://doi.org/10.2307/1543169
Stat, M., Loh, W., Hoegh-Guldberg, O., & Carter, D. (2008). Symbiont acquisition strategy drives host-symbiont associations in the southern Great Barrier Reef. Coral Reefs, 27(4), 763-772. https://doi.org/10.1007/s00338-008-0412-5
Stat, M., Loh, W., LaJeunesse, T., Hoegh-Guldberg, O., & Carter, D. (2009). Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs, 28(3), 709-713. https://doi.org/10.1007/s00338-009-0509-5
Stat, M., Pochon, X., Cowie, R. O., & Gates, R. D. (2009). Specificity in communities of Symbiodinium in corals from Johnston Atoll. Marine Ecology Progress Series, 386, 83-96. https://doi.org/10.3354/meps08080
Stern, R. F., Horak, A., Andrew, R. L., Coffroth, M.-A., Andersen, R. A., Küpper, F. C., Jameson, I., Hoppenrath, M., Véron, B., Kasai, F., Brand, J., James, E. R., & Keeling, P. J. (2010). Environmental barcoding reveals massive dinoflagellate diversity in marine environments. PLoS One, 5(11), e13991. https://doi.org/10.1371/journal.pone.0013991
Suggett, D. J., Goyen, S., Evenhuis, C., Szabó, M., Pettay, D. T., Warner, M. E., & Ralph, P. J. (2015). Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytologist, 208(2), 370-381.
Sweet, M. J. (2014). Symbiodinium diversity within Acropora muricata and the surrounding environment. Marine Ecology, 35(3), 343-353.
Takabayashi, M., Adams, L., Pochon, X., & Gates, R. (2012). Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai 'i and Florida. Coral Reefs, 31(1), 157-167. https://doi.org/10.1007/s00338-011-0832-5
Thomas, L., Kendrick, G., Kennington, W., Richards, Z., & Stat, M. (2014). Exploring Symbiodinium diversity and host specificity in Acropora corals from geographical extremes of Western Australia with 454 amplicon pyrosequencing. Molecular Ecology, 23(12), 3113-3126.
Thornhill, D., Lajeunesse, T., & Santos, S. (2007). Measuring rDNA diversity in eukaryotic microbial systems: How intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Molecular Ecology, 16(24), 5326-5340. https://doi.org/10.1111/j.1365-294X.2007.03576.x
Thornhill, D., Lewis, A. M., Wham, D. C., & LaJeunesse, T. C. (2014). Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution, 68(2), 352-367. https://doi.org/10.1111/evo.12270
Thornhill, D., Michael, W., LaJeunesse, T., Schmidt, G. W., & Fitt, W. K. (2006). Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. Journal of Experimental Marine Biology and Ecology, 338(1), 50-56. https://doi.org/10.1016/j.jembe.2006.06.032
Ulstrup, K. E., Hill, R., Van Oppen, M., Larkum, A., & Ralph, P. (2008). Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals. Marine Ecology Progress Series, 361, 139-150. https://doi.org/10.3354/meps07360
Venera-Ponton, D., Diaz-Pulido, G., Rodriguez-Lanetty, M., & Hoegh-Guldberg, O. (2010). Presence of Symbiodinium spp. in macroalgal microhabitats from the southern Great Barrier Reef. Coral Reefs, 29(4), 1049-1060.
Wada, S., Aoki, M. N., Tsuchiya, Y., Sato, T., Shinagawa, H., & Hama, T. (2007). Quantitative and qualitative analyses of dissolved organic matter released from Ecklonia cava Kjellman, in Oura Bay, Shimoda, Izu Peninsula, Japan. Journal of Experimental Marine Biology and Ecology, 349(2), 344-358. https://doi.org/10.1016/j.jembe.2007.05.024
Wang, J.-T., Meng, P.-J., Sampayo, E., Tang, S.-L., & Chen, C. (2011). Photosystem II breakdown induced by reactive oxygen species in freshly-isolated Symbiodinium from Montipora (Scleractinia; Acroporidae). Marine Ecology Progress Series, 422, 51-62. https://doi.org/10.3354/meps08913
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261-5267.
Winkler, N. S., Pandolfi, J. M., & Sampayo, E. M. (2015). Symbiodinium identity alters the temperature-dependent settlement behaviour of Acropora millepora coral larvae before the onset of symbiosis. Proceedings of the Royal Society B: Biological Sciences, 282(1801), 20142260.
Wright, E. S. (2016). Using DECIPHER v2. 0 to analyze big biological sequence data in R. R Journal, 8(1), 352-359.
Yamashita, H., & Koike, K. (2013). Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycological Research, 61(1), 68-80.
Yamashita, H., Suzuki, G., Hayashibara, T., & Koike, K. (2011). Do corals select zooxanthellae by alternative discharge? Marine Biology, 158(1), 87-100. https://doi.org/10.1007/s00227-010-1544-z
Yamashita, H., Suzuki, G., Hayashibara, T., & Koike, K. (2013). Acropora recruits harbor “rare” Symbiodinium in the environmental pool. Coral Reefs, 32(2), 355-366. https://doi.org/10.1007/s00338-012-0980-2
Yamashita, H., Suzuki, G., Kai, S., Hayashibara, T., & Koike, K. (2014). Establishment of coral-algal symbiosis requires attraction and selection. PLoS One, 9(5), e97003. https://doi.org/10.1371/journal.pone.0097003
Ziegler, M., Arif, C., Burt, J. A., Dobretsov, S., Roder, C., LaJeunesse, T., & Voolstra, C. R. (2017). Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. Journal of Biogeography, 44(3), 674-686.