Cladocopium infistulum sp. nov. (Dinophyceae), a thermally tolerant dinoflagellate symbiotic with giant clams from the western Pacific Ocean

REFERENCES

• Abrego D., Ulstrup K.E., Willis B.L. & Van Oppen M.J. 2008. Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress. Proceedings of the Royal Society B: Biological Sciences 275: 2273–2282. DOI: 10.1098/rspb.2008.0180.
   PubMed Web of Science ®Google Scholar
• Baillie B.K., Belda–Baillie C.A. & Maruyama T. 2000. Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. Journal of Phycology 36: 1153–1161. DOI: 10.1046/j.1529-8817.2000.00010.x.
   Web of Science ®Google Scholar
• Carlos A.A., Baillie B.K. & 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: 1054–1062. DOI: 10.1046/j.1529-8817.1999.3551054.x.
   Web of Science ®Google Scholar
• Chen C.A., Yang Y.-W., Wei N.V., 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. DOI: 10.1007/s00338-004-0389-7.
   Web of Science ®Google Scholar
• DeBoer T.S., Baker A.C., Erdmann M.V., Ambariyanto A., Jones P.R. & Barber P.H. 2012. Patterns of Symbiodinium distribution in three giant clam species across the biodiverse Bird’s Head region of Indonesia. Marine Ecology Progress Series 444: 117–132. DOI: 10.3354/meps09413.
   Web of Science ®Google Scholar
• Diaz-Almeyda E.M., Prada C., Ohdera A.H., Moran H., Civitello D.J., Iglesias-Prieto R., Carlo T.A., LaJeunesse T.C. & Medina M. 2017. Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proceedings of the Royal Society B: Biological Sciences 284: 20171767. DOI: 10.1098/rspb.2017.1767.
   Web of Science ®Google Scholar
• Fisher P.L., Malme M.K. & Dove S. 2011. The effect of temperature stress on coral–Symbiodinium associations containing distinct symbiont types. Coral Reefs 31: 473–485. DOI: 10.1007/s00338-011-0853-0.
   Web of Science ®Google Scholar
• Golbuu Y., Victor S., Penland L., Idip J.D., Emaurois C., Okaji K., Yukihira H., Iwase A. & van Woesik R. 2007. Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26: 319–332. DOI: 10.1007/s00338-007-0200-7.
   Web of Science ®Google Scholar
• Grégoire V., Schmacka F., Coffroth M.A. & Karsten U. 2017. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). Journal of Applied Phycology 29: 1893–1905. DOI: 10.1007/s10811-017-1127-1.
   Web of Science ®Google Scholar
• Holt A.L., Vahidinia S., Gagnon Y.L., Morse D.E. & Sweeney A.M. 2014. Photosymbiotic giant clams are transformers of solar flux. Journal of the Royal Society Interface 11: 20140678. DOI: 10.1098/rsif.2014.0678.
   Web of Science ®Google Scholar
• Hume B.C.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: 8562. DOI: 10.1038/srep08562.
   PubMed Web of Science ®Google Scholar
• Hume B.C.C., D’Angelo C., Smith E.G., Stevens J.R., Burt J.A. & Wiedenmann J. 2018. Validation of the binary designation Symbiodinium thermophilum (Dinophyceae). Journal of Phycology 54: 762–764. DOI: 10.1111/jpy.12764.
   Web of Science ®Google Scholar
• Klumpp D.W. & Griffiths C.L. 1994. Contributions of phototrophic and heterotrophic nutrition to the metabolic and growth requirements of four species of giant clam (Tridacnidae). Marine Ecology Progress Series 115: 103–115. DOI: 10.3354/meps115103.
   Web of Science ®Google Scholar
• 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. DOI: 10.1016/j.jembe.2011.12.002.
   Web of Science ®Google Scholar
• LaJeunesse T., Thornhill D., Cox E., Stanton F., Fitt W. & Schmidt G. 2004a. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23: 596–603.
   Web of Science ®Google Scholar
• LaJeunesse T.C. 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: 866–880. DOI: 10.1046/j.1529-8817.2001.01031.x.
   Web of Science ®Google Scholar
• LaJeunesse T.C. 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141: 387–400. DOI: 10.1007/s00227-002-0829-2.
   Web of Science ®Google Scholar
• LaJeunesse T.C. 2005. “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Molecular Biology and Evolution 22: 570–581. DOI: 10.1093/molbev/msi042.
   PubMed Web of Science ®Google Scholar
• LaJeunesse T.C., Bhagooli R., Hidaka M., DeVantier L., Done T., Schmidt G.W., Fitt W.K. & Hoegh-Guldberg O. 2004b. 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. DOI: 10.3354/meps284147.
   Web of Science ®Google Scholar
• LaJeunesse T.C., Fitt W.K. & Schmidt G.W. 2010a. The reticulated chloroplasts of zooxanthellae (Symbiodinium) and differences in chlorophyll localization among life cycle stages. Coral Reefs 29: 627. DOI: 10.1007/s00338-010-0635-0.
   Web of Science ®Google Scholar
• LaJeunesse T.C., Loh W.K.W., 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: 2046–2054. DOI: 10.4319/lo.2003.48.5.2046.
   Web of Science ®Google Scholar
• LaJeunesse T.C., 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: 2570–2580. DOI: 10.1016/j.cub.2018.07.008.
   PubMed Web of Science ®Google Scholar
• LaJeunesse T.C., Pettay D.T., Sampayo E.M., Phongsuwan N., Brown B., Obura D.O., Hoegh-Guldberg O. & Fitt W.K. 2010b. 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. Journal of Biogeography 37: 785–800. DOI: 10.1111/j.1365-2699.2010.02273.x.
   Web of Science ®Google Scholar
• LaJeunesse T.C. & Trench R.K. 2000. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biological Bulletin 199: 126–134. DOI: 10.2307/1542872.
   PubMed Web of Science ®Google Scholar
• Lee S.Y., Jeong H.J., Kang N.S., Jang T.Y., Jang S.H. & LaJeunesse T.C. 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. European Journal of Phycology 50: 155–172. DOI: 10.1080/09670262.2015.1018336.
   Web of Science ®Google Scholar
• Leliaert F., Verbruggen H., Vanormelingen P., Steen F., López-Bautista J.M., Zuccarello G.C. & De Clerck O. 2014. DNA-based species delimitation in algae. European Journal of Phycology 49: 179–196. DOI: 10.1080/09670262.2014.904524.
   Web of Science ®Google Scholar
• Lobban C.S., Schefter M., Simpson A.G.B., Pochon X., Pawlowski J. & Foer W. 2002. Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands. Marine Biology 140: 411–423. DOI: 10.1007/s002270100690.
   Web of Science ®Google Scholar
• Moore R.B., Ferguson K.M., Loh W.K., Hoegh-Guldberg O. & Carter D.A. 2003. Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. International Journal of Systematic and Evolutionary Microbiology 53: 1725–1734. DOI: 10.1099/ijs.0.02594-0.
   PubMed Web of Science ®Google Scholar
• Nitschke M.R., Craveiro S.C., Brandao C., Fidalgo C., Serodio 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 56: 923–940. DOI: 10.1111/jpy.12999.
   Web of Science ®Google Scholar
• Norton J.H., Shepperd M.A., Long H.M. & Fitt W.K. 1992. The zooxanthellal tubular system in the giant clam. Biological Bulletin 183: 503–506. DOI: 10.2307/1542028.
   PubMed Web of Science ®Google Scholar
• Pochon X., LaJeunesse T.C. & Pawlowski J. 2004. Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Marine Biology 146: 17–27. DOI: 10.1007/s00227-004-1427-2.
   Web of Science ®Google Scholar
• Rodriquez-Lanetty M., Krupp D.A. & Weis V.M. 2004. Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Marine Ecology Progress Series 275: 97–102. DOI: 10.3354/meps275097.
   Web of Science ®Google Scholar
• Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu L., Suchard M.A. & Huelsenbeck J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. DOI: 10.1093/sysbio/sys029.
   PubMed Web of Science ®Google Scholar
• Rosewater J. 1965. The family Tridacnidae in the Indo-Pacific. Department of Mollusks, Academy of Natural Sciences of Philadelphia. 62 pp.
   Google Scholar
• Rowan R., Whitney S.M., Fowler A. & Yellowlees D. 1996. Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8: 539–553. DOI: 10.1105/tpc.8.3.539.
   PubMed Web of Science ®Google Scholar
• Sampayo E.M., Dove S. & LaJeunesse T.C. 2009. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Molecular Ecology 18: 500–519. DOI: 10.1111/j.1365-294X.2008.04037.x.
   PubMed Web of Science ®Google Scholar
• Sampayo E.M., Franceschinis L., Hoegh-Guldberg O. & Dove S. 2007. Niche partitioning of closely related symbiotic dinoflagellates. Molecular Ecology 16: 3721–3733. DOI: 10.1111/j.1365-294X.2007.03403.x.
   Web of Science ®Google Scholar
• Sampayo E.M., Ridgway T., Bongaerts P. & Hoegh-Guldberg O. 2008. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of the National Academy of Sciences USA 105: 10444–10449. DOI: 10.1073/pnas.0708049105.
   PubMed Web of Science ®Google Scholar
• 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: 900–912. DOI: 10.1046/j.1529-8817.2001.00194.x.
   Web of Science ®Google Scholar
• Schnieder C.A., Rasband W.S. & Eliceiri K.W. 2012. NIH image to imageJ: 25 years of image analysis. Nature Methods 9: 671–675. DOI: 10.1038/nmeth.2089.
   Web of Science ®Google Scholar
• Seutin G., White B.N. & Boag P.T. 1991. Preservation of avian blood and tissue samples for DNA analysis. Canadian Journal of Zoology 69: 82–90. DOI: 10.1139/z91-013.
   Web of Science ®Google Scholar
• Shamberger K.E.F., Cohen A.L., Golbuu Y., McCorkle D.C., Lentz S.J. & Barkley H.C. 2014. Diverse coral communities in naturally acidified waters of a Western Pacific reef. Geophysical Research Letters 41: 499–504. DOI: 10.1002/2013GL058489.
   Web of Science ®Google Scholar
• Suggett D.J., Goyen S., Evenhuis C., Szabo 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: 370–381. DOI: 10.1111/nph.13483.
   Web of Science ®Google Scholar
• Swofford D.L. 2014. PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, Massachusetts, USA.
   Google Scholar
• Thomas M.K., Kremer C.T., Klausmeir C.A. & Litchman E. 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338: 1085–1088. DOI: 10.1126/science.1224836.
   PubMed Web of Science ®Google Scholar
• Thornhill D.J., Lewis A.M., Wham D.C. & LaJeunesse T.C. 2014. Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68: 352–367. DOI: 10.1111/evo.12270.
   PubMed Web of Science ®Google Scholar
• Trench R.K. & Blank R.J. 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. DOI: 10.1111/j.1529-8817.1987.tb02534.x.
   Web of Science ®Google Scholar
• Trench R.K., Wethey D.S. & Porter J.W. 1981. Observations on the symbiosis with zooxanthellae among the Tridacnidae (Mollusca, Bivalvia). Biological Bulletin 161: 180–198. DOI: 10.2307/1541117.
   Web of Science ®Google Scholar
• Turland N.J., Wiersema J.H., Barrie F.R., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Kusber W.-H., Li D.-Z. & Marhold K. et al. (eds.) 2018. International code of nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Koeltz Botanical Books, Glashütten, Germany. DOI: 10.12705/Code.2018.
   Google Scholar
• Van Oppen M.J., Mieog J.C., Sanchez C.A. & Fabricius K.E. 2005. Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Molecular Ecology 14: 2403–2417. DOI: 10.1111/j.1365-294X.2005.02545.x.
   PubMed Web of Science ®Google Scholar
• Weber M.X. 2009. The biogeography and evolution of Symbiodinium in giant clams (Tridacnidae). In: Integrative biology UC Berkeley, pp. 119. University of California, Berkeley, California, USA.
   Google Scholar
• Zardoya R., Costas E., Lopez-Rodas V., Garrido-Pertierra A. & Bautista J.M. 1995. Revised dinoflagellate phylogeny inferred from molecular analysis of large-subunit ribosomal RNA gene sequences. Journal of Molecular Evolution 41: 637–645. DOI: 10.1007/BF00175822.
   PubMed Web of Science ®Google Scholar
• Zhang H., Bhattacharya D., Maranda L. & Lin S. 2008. Mitochondrial cob and cox1 genes and editing of the corresponding mRNAs in Dinophysis acuminata from Narragansett Bay, with special reference to the phylogenetic position of the genus Dinophysis. Applied Environmental Microbiology 74: 1546–1554. DOI: 10.1128/AEM.02103-07.
   PubMed Web of Science ®Google Scholar
• Zhang Z., Green B.R. & Cavalier-Smith T. 2000. Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. Journal of Molecular Evolution 51: 26–40. DOI: 10.1007/s002390010064.
   PubMed Web of Science ®Google Scholar
• Ziegler M., Arif C., Burt J.A., Dobretsov S., Roder C., LaJeunesse T.C. & Voolstra C.R. 2017. Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. Journal of Biogeography 44: 674–686. DOI: 10.1111/jbi.12913.
   Web of Science ®Google Scholar