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

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Abstract

Elevated temperatures can produce a range of serious, deleterious effects on marine invertebrate—Symbiodinium symbioses. The responses of free-living Symbiodinium to elevated temperature, however, have been little studied, especially in the context of their natural habitat. In this study, we investigated physiological responses of two Symbiodinium cultures to elevated temperature, an exclusively free-living ITS2 clade A (strain HI-0509) and the symbiosis-forming ITS2 type A1 (strain CCMP2467). Free-living Symbiodinium strains have recently been isolated from benthic sediments, and both cultures were therefore grown with or without a microhabitat of carbonate sediment at 25, 28 or 31 °C. Maximum quantum yield of photosystem II (F v/F m) and specific growth rate were measured as response variables. In culture, Symbiodinium cells exhibit motility in a helical swimming pattern, and therefore, revolutions per minute (RPM) were also measured with video microscopy. The exclusively free-living clade A was physiologically superior to Symbiodinium A1 across all measured variables and treatment combinations. F v/F m remained relatively stable through time (at approximately 0.55) and was not substantially affected by temperature or the presence or the absence of sediment. Populations of the exclusively free-living Symbiodinium A reproduced faster with sediment than without and exhibited high levels of motility across all treatments (surpassing 300 RPM). In contrast, the F v/F m of A1 dropped to 0.42 in sediment (relative to cultures without sediment) and exhibited dramatic declines in cell concentration, most severely at 31 °C. A > 50 % reduction in motility was also observed at 31 °C. Even in the absence of sediment, elevated temperature was observed to reduce population growth and cell motility of type A1. We suggest that vital behaviours linked to motility (such as vertical migration and the locating of potential hosts) may become impaired during future thermal anomalies and that populations of Symbiodinium A1 may only live transiently in sediment or outside coral hosts. Such differences in physiology between distinct Symbiodinium types may represent adaptations that are either conserved or lost depending on the differing selection pressures that come with living in symbiosis or free in the environment.

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References

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cumbo VR, Baird AH, van Oppen MJH (2013) The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:111–120

    Article  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709

    Article  CAS  Google Scholar 

  • Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Global Change Biol 19:3640–3647

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Freudenthal HD (1962) Symbiodinium gen. nov. and Symbiodinium sp. nov., a Zooxanthella: Taxonomy, Life Cycle, and Morphology.*. J Protozool 9:45–52

    Article  Google Scholar 

  • Guillard R (1973) Division Rates Handbook of Phycological Methods - Culture Methods and Growth Measurements. Cambridge University Press, New York, pp 298–311

    Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclothella nana Hustedt, and Detonula confervacea (cleve) Gran. Can J Microbiol 229–239

  • Hawkins TD, Davy SK (2012) Nitric oxide production and tolerance differ among Symbiodinium types exposed to heat stress. Plant Cell Physiol 53:1889–1898

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hill R, Ralph P (2007) Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 352:137–144

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86

    Article  Google Scholar 

  • Ichimi K, Tada K, Montani S (2008) Simple estimation of penetration rate of light in intertidal sediments. J Oceanogr 64:399–404

    Article  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kamykowski D, McCollum SA (1986) The temperature acclimatized swimming speed of selected marine dinoflagellates. J Plankton Res 8:275–287

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Article  Google Scholar 

  • LaJeunesse TC, Loh W, Trench RK (2009) Do introduced endosymbiotic dinoflagellates ‘take’ to new hosts? Biol Invasions 11:995–1003

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Massaro RS, Carlo E, Drupp P, Mackenzie F, Jones S, Shamberger K, Sabine C, Feely R (2012) Multiple factors driving variability of CO2 exchange between the ocean and atmosphere in a tropical coral reef environment. Aquat Geochem 18:357–386

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • McMinn A, Martin A (2013) Dark survival in a warming world. Proc R Soc Biol Sci Ser B 280:20122909

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Pasternak Z, Blasius B, Abelson A, Achituv Y (2006) Host-finding behaviour and navigation capabilities of symbiotic zooxanthellae. Coral Reefs 25:201–207

    Article  Google Scholar 

  • 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

  • Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Sinclair GA, Kamykowski D (2008) Benthic-pelagic coupling in sediment-associated populations of Karenia brevis. J Plankton Res 30:829–838

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Stat M, Gates RD (2008) Vectored introductions of marine endosymbiotic dinoflagellates into Hawaii. Biol Invasions 10:579–583

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank Thomas Krüger for providing Symbiodinium cultures and assisting with the experimental setup. We are also grateful to members of the Davy Lab for discussions about these data and protocol assistance. Two anonymous reviewers contributed to a revised edition of this manuscript, and we are thankful for this. Sediment collection was conducted under the conditions described in GBRMPA permit number G12/35077.1. This experiment was supported through funding awarded to SW and, in part, by a Royal Society of New Zealand Marsden Fund grant (contract number VUW0902) to SKD.

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Correspondence to M. R. Nitschke.

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Nitschke, M.R., Davy, S.K., Cribb, T.H. et al. The effect of elevated temperature and substrate on free-living Symbiodinium cultures. Coral Reefs 34, 161–171 (2015). https://doi.org/10.1007/s00338-014-1220-8

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  • DOI: https://doi.org/10.1007/s00338-014-1220-8

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