The effect of elevated temperature and substrate on free-living Symbiodinium cultures

Coral Reefs

Volumn 34, Issue 1, 2015, Pages 161-171

  Nitschke, M R ^a   Davy, S K ^b   Cribb, T H ^a   Ward, S ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Free living; Growth; Motility; Photosynthesis; Sediment; Symbiodinium

Indexed keywords

EID: 84925536587     PISSN: 07224028     EISSN: 14320975     Source Type: Journal    
DOI: 10.1007/s00338-014-1220-8     Document Type: Article

References (64)

1. Adams LM, Cumbo VR, Takabayashi M (2009) Exposure to sediment enhances primary acquisition of Symbiodinium by asymbiotic coral larvae. Mar Ecol Prog Ser 377:149–156
2. 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
3. Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Evol Syst 40:551–571
4. Bongaerts P, Sampayo EM, Bridge TCL, Ridgway T, Vermeulen F, Englebert N, Webster JM, Hoegh-Guldberg O (2011) Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment. Mar Ecol Prog Ser 439:117–126
5. Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99–105
6. Byler KA, Carmi-Veal M, Fine M, Goulet TL (2013) Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS One 8:e59596
7. Carlos AA, Baillie BK, 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. J Phycol 35:1054–1062
8. Coffroth MA, Lewis CF, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol 16:R985–R987
9. Correa AMS, Baker AC (2009) Understanding diversity in coral-algal symbiosis: a cluster-based approach to interpreting fine-scale genetic variation in the genus Symbiodinium. Coral Reefs 28:81–93
10. Cumbo VR, Baird AH, van Oppen MJH (2013) The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–120
11. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709
12. Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Global Change Biol 19:3640–3647
13. Fisher PL, Malme MK, Dove S (2012) The effect of temperature stress on coral-Symbiodinium associations containing distinct symbiont types. Coral Reefs 31:473–485
14. Fitt WK (1984) The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and mollusks with zooxanthellae. Mar Biol 81:9–17
15. Fitt WK, Trench RK (1983) The relation of diel patterns of cell-division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal in culture. New Phytol 94:421–432
16. Fitt WK, Chang SS, Trench RK (1981) Motility patterns of different strains of the symbiotic dinoflagellate Symbiodinium (=Gymnodinium) microadriaticum (Freudenthal) in culture. Bull Mar Sci 31:436–443
17. Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium-host symbioses. Mol Ecol Resour 12:369–373
18. Freudenthal HD (1962) Symbiodiniumgen. nov. and Symbiodinium sp. nov., a Zooxanthella: Taxonomy, Life Cycle, and Morphology.*. J Protozool 9:45–52
19. Guillard R (1973) Division Rates Handbook of Phycological Methods - Culture Methods and Growth Measurements. Cambridge University Press, New York, pp 298–311
20. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclothella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 229–239
21. Hawkins TD, Davy SK (2012) Nitric oxide production and tolerance differ among Symbiodinium types exposed to heat stress. Plant Cell Physiol 53:1889–1898
22. 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
23. Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195
24. Hill R, Ralph P (2007) Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 352:137–144
25. Hill R, Brown CM, DeZeeuw K, Campbell DA, Ralph PJ (2011) Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo-inactivation. Limnol Oceanogr 56:139–146
26. 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
27. Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86
28. Ichimi K, Tada K, Montani S (2008) Simple estimation of penetration rate of light in intertidal sediments. J Oceanogr 64:399–404
29. Jeong HJ, Yoo YD, Kang NS, Lim AS, Seong KA, Lee SY, Lee MJ, Lee KH, Kim HS, Shin W, Nam SW, Yih W, Lee K (2012) Heterotrophic feeding as a newly identified survival strategy of the dinoflagellate Symbiodinium. Proc Natl Acad Sci U S A 109:12604–12609
30. Kamykowski D, McCollum SA (1986) The temperature acclimatized swimming speed of selected marine dinoflagellates. J Plankton Res 8:275–287
31. Krämer WE, Caamano-Ricken I, Richter C, Bischof K (2012) Dynamic regulation of photoprotection determines thermal tolerance of two phylotypes of Symbiodinium clade A at two photon fluence rates. Photochem Photobiol 88:398–413
32. Krueger T, Gates RD (2012) Cultivating endosymbionts - Host environmental mimics support the survival of Symbiodinium C15 ex hospite. J Exp Mar Biol Ecol 413:169–176
33. Kühl M, Lassen C, Jorgensen BB (1994) Light penetration and light-intensity in sandy marine-sediments measured with irradiance and scalar irradiance fiberoptic microprobes. Mar Ecol Prog Ser 105:139–148
34. 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
35. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
36. LaJeunesse TC, Loh W, Trench RK (2009) Do introduced endosymbiotic dinoflagellates ‘take’ to new hosts? Biol Invasions 11:995–1003
37. Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377
38. Lewis J, Harris ASD, Jones KJ, Edmonds RL (1999) Long-term survival of marine planktonic diatoms and dinoflagellates in stored sediment samples. J Plankton Res 21:343–354
39. 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
40. Lundholm N, Ribeiro S, Andersen TJ, Koch T, Godhe A, Ekelund F, Ellegaard M (2011) Buried alive - germination of up to a century-old marine protist resting stages. Phycologia 50:629–640
41. 2 exchange between the ocean and atmosphere in a tropical coral reef environment. Aquat Geochem 18:357–386
42. McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007
43. McKay L, Kamykowski D, Milligan E, Schaeffer B, Sinclair G (2006) Comparison of swimming speed and photophysiological responses to different external conditions among three Karenia brevis strains. Harmful Algae 5:623–636
44. McMinn A, Martin A (2013) Dark survival in a warming world. Proc R Soc Biol Sci Ser B 280:20122909
45. Mellas RE, McIlroy SE, Fitt WK, Coffroth MA (2014) Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp. J Exp Mar Biol Ecol 459:38–44
46. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world: Coral reefs. Elsevier, Amsterdam, pp 75–87
47. Pasternak Z, Blasius B, Abelson A, Achituv Y (2006) Host-finding behaviour and navigation capabilities of symbiotic zooxanthellae. Coral Reefs 25:201–207
48. Paterson D, Hagerthey S (2001) Microphytobenthos in contrasting coastal ecosystems: biology and dynamics. In Reise (ed) Ecological comparisons of sedimentary shores. Springer, pp 105–125
49. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497
50. 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 46:53–65
51. Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 406:57–70
52. Reimer JD, Shah MMR, Sinniger F, Yanagi K, Suda S (2010) Preliminary analyses of cultured Symbiodinium isolated from sand in the oceanic Ogasawara Islands, Japan. Mar Biodiv 40:237–247
53. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals - Comparisons among the Caribbean, the tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203
54. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579
55. Rodrigues LJ, Grottoli AG, Lesser MP (2008) Long-term changes in the chlorophyll fluorescence of bleached and recovering corals from Hawaii. J Exp Biol 211:2502–2509
56. Sinclair GA, Kamykowski D (2008) Benthic-pelagic coupling in sediment-associated populations of Karenia brevis. J Plankton Res 30:829–838
57. Sorek M, Levy O (2012) The effect of temperature compensation on the circadian rhythmicity of photosynthesis in Symbiodinium, coral-symbiotic alga. Sci Rep 2:536
58. Starzak DE, Quinnell RG, Nitschke MR, Davy SK (2014) The influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis. Mar Biol 161:711–724
59. Stat M, Gates RD (2008) Vectored introductions of marine endosymbiotic dinoflagellates into Hawaii. Biol Invasions 10:579–583
60. Takabayashi M, Adams LM, Pochon X, Gates RD (2012) Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai’i and Florida. Coral Reefs 31:157–167
61. Venera-Ponton DE, 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 29:1049–1060
62. Yacobovitch T, Benayahu Y, Weis VM (2004) Motility of zooxanthellae isolated from the Red Sea soft coral Heteroxenia fuscescens (Cnidaria). J Exp Mar Biol Ecol 298:35–48
63. Yamashita H, Koike K (2013) Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res 61:68–80
64. Yang SY, Keshavmurthy S, Obura D, Sheppard CRC, Visram S, Chen CA (2012) Diversity and distribution of Symbiodinium associated with seven common coral species in the Chagos archipelago, Central Indian Ocean. PLoS One 7:1–9