Dimethylsulphoniopropionate (DMSP) as an Indicator of Bleaching Tolerance in Scleractinian Corals

Journal of Marine Science and Engineering - Tập 3 Số 2 - Trang 444-465
Graham B. Jones1, Stacey King1
1Marine Ecology Research Centre, School of Environment, Science and Engineering, Southern Cross University, Lismore, NSW, 2480, Australia

Tóm tắt

Thermal tolerance tests on Acropora millepora, a common Indo-Pacific hard coral, have shown that adult corals can acquire increased thermal tolerance by shuffling existing type C to type D Symbiodinium zooxanthellae when subjected to increased seawater temperatures. We report here dimethylsulphoniopropionate (DMSP) concentrations in A. millepora and examine links between DMSP concentrations, zooxanthellae clade, and bleaching tolerance. DMSP analysis on native and transplanted corals from three locations in the Great Barrier Reef indicated that the lower thermal tolerance in type C zooxanthellae coincided with variable DMSP concentrations, whilst the more thermal tolerant type D zooxanthellae had more stable areal DMSP concentrations as seawater temperatures increased. Our results suggest this increased thermal tolerance in type D zooxanthellae may reflect the ability of these coral symbionts to conserve their antioxidant DMSP levels to relatively constant concentrations, enabling the coral to overcome the build-up of oxygen free radicals in the cytoplasm of A. millepora. A conceptual diagram illustrates how the antioxidants DMS (P) participate in the bleaching process by scavenging oxygen free radicals and form DMSO, thus moderating coral bleaching and increasing thermotolerance.

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Tài liệu tham khảo

Berkelmans, 1999, Large-scale bleaching of corals on the Great Barrier Reef, Coral Reefs, 18, 55, 10.1007/s003380050154

Harriot, 1985, Mortality rates of scleractinian corals before and during a mass bleaching event, Mar. Ecol. Prog. Ser., 21, 81, 10.3354/meps021081

Jones, 1997, Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event, Mar. Ecol. Prog. Ser., 158, 51, 10.3354/meps158051

Jones, 1997, Zooxanthellae loss as a bioassay for assessing stress in corals, Mar. Ecol. Prog. Ser., 149, 163, 10.3354/meps149163

Jones, 1997, Recurrent bleaching of corals at Magnetic Island (Australia) relative to air and seawater temperature, Mar. Ecol. Prog. Ser., 158, 289, 10.3354/meps158289

Berkelmans, 2004, A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: Spatial correlation, patterns, and predictions, Coral Reefs, 23, 74, 10.1007/s00338-003-0353-y

1999, Climate change, coral bleaching and the future of the world's coral reefs, Mar. Freshw. Res., 50, 839

Brown, 1995, Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event, Mar. Biol., 122, 655, 10.1007/BF00350687

Douglas, 2003, Coral bleaching-how and why?, Mar. Poll. Bull., 46, 385, 10.1016/S0025-326X(03)00037-7

Ahern, H., Ahmad, S., Birnbaum, M.R., Cadenas, E., Chen, Y., Cunningham, R.P., Dalton, D.A., Felton, G.W., Grisham, M.B., and Kalyanaraman, B. (1995). Oxidative Stress and Antioxidant Defenses in Biology, Chapman & Hall.

Fridovich, 1978, The biology of oxygen radicals, Science, 201, 875, 10.1126/science.210504

Dykens, 1982, Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host, Nature, 297, 579, 10.1038/297579a0

Franklin, 2004, Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching, Mar. Ecol. Prog. Ser., 272, 117, 10.3354/meps272117

Lesser, 1996, Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates, Limnol. Oceanogr., 41, 271, 10.4319/lo.1996.41.2.0271

Downs, 2002, Oxidative stress and seasonal coral bleaching, Free Radic. Biol. Med., 33, 533, 10.1016/S0891-5849(02)00907-3

Jones, 1998, Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae, Plant Cell Environ., 21, 1219, 10.1046/j.1365-3040.1998.00345.x

Lesser, 1990, Bleaching in coral reef anthozoans: Effect of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen, Coral Reefs, 8, 225, 10.1007/BF00265015

Rowan, 1991, Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae), Mar. Ecol. Prog. Ser., 71, 65, 10.3354/meps071065

Greenwood, J.G., and Hall, N.J. (, January October). Diversity of zooxanthellae from scleractinian corals of One Tree Island (The Great Barrier Reef). Proceedings of the Australian Coral Reef Society 75th Anniversary Conference, School of Marine Science, University of Queensland, Brisbane, Heron Island, Austrilia.

Baker, 2001, Reef corals bleach to survive change, Nature, 411, 765, 10.1038/35081151

Rowan, 1997, Landscape ecology of algal symbionts creates variation in episodes of coral bleaching, Nature, 388, 265, 10.1038/40843

Berkelmans, 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. R. Soc. B, 273, 2305, 10.1098/rspb.2006.3567

Chen, 2003, A stable association of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature-tolerant coral, Oulastrea crispate (Scleractinia: Faviidae) in subtropical non-reefal coral communities, Zool. Stud., 42, 540

Buddemeier, 1993, Coral bleaching as an adaptive mechanism: A testable hypothesis, Bioscience, 43, 320, 10.2307/1312064

Sunda, 2002, An antioxidant function for DMSP and DMS in marine algae, Nature, 418, 317, 10.1038/nature00851

Lee, 1999, Intracellular dimethylsulfoxide (DMSO) in unicellular marine algae: Speculations on its origin and possible biological role, J. Phycol., 35, 8, 10.1046/j.1529-8817.1999.3510008.x

Broadbent, 2002, DMSP in corals and benthic algae from the Great Barrier Reef, Estuar. Coast. Shelf Sci., 55, 547, 10.1006/ecss.2002.1021

Hill, 1995, Dimethylsulfoniopropionate in Reef Corals, B Mar. Sci., 57, 489

Bellwood, O., Choat, H., and Saxena, N. (1994). Recent Advances in Marine Science and Technology, Pacon International and James Cook University of North Queensland.

Broadbent, 2004, DMS and DMSP in mucus ropes, coral mucus, surface films and sediment pore waters from coral reefs in the Great Barrier Reef, Mar. Freshw. Res., 55, 849, 10.1071/MF04114

Deschaseaux, 2014, Effects of environmental factors on dimethylated sulfur compounds and their potential role in the antioxidant system of the coral holobiont, Limnol. Oceanogr., 59, 758, 10.4319/lo.2014.59.3.0758

Fischer, 2012, Atmospheric dimethysulphide production from corals in the Great Barrier Reef and links to solar radiation, climate and coral bleaching, Biogeochemistry, 110, 31, 10.1007/s10533-012-9719-y

Narchi, N., and Price, L. (2015). The Reef Sulphur Cycle: Influence on Climate and Ecosystem Services, Springer. (in press).

Jones, 2005, The influence of coral reefs on atmospheric dimethylsulphide over the Great Barrier Reef, Coral Sea, Gulf of Papua, Solomon and Bismarck Seas, Mar. Freshw. Res., 56, 85, 10.1071/MF04097

Modini, 2009, New particle formation and growth at a remote, sub-tropical coastal location, Atmos. Chem. Phys. Discuss., 9, 12101

Swan, H., Jones, G., and Deschaseaux, E. (2012, January 9–13). Dimethylsulfide and coral reef ecosystems. Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia.

Raina, 2013, DMSP biosynthesis by an animal and its role in coral thermal stress response, Nature, 502, 677, 10.1038/nature12677

Deschaseaux, 2014, Comparative response of DMS and DMSP concentrations in Symbiodinium clades C1 and D1 under thermal stress, J. Exp. Mar. Biol. Ecol., 459, 181, 10.1016/j.jembe.2014.05.018

Jones, 2014, The effect of coral bleaching on the cellular concentration of dimethylsulphoniopropionate in reef corals, J. Exp. Mar. Biol. Ecol., 460, 19, 10.1016/j.jembe.2014.06.003

Berkelmans, 2002, Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef, Mar. Ecol. Prog. Ser., 229, 73, 10.3354/meps229073

Turner, 2002, Precise set-point control of temperature for coral bleaching experiments, Mar. Technol. Soc. J., 36, 70, 10.4031/002533202787914160

Ulstrup, 2003, Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef, Mol. Ecol., 12, 3477, 10.1046/j.1365-294X.2003.01988.x

Palstra, 2001, Patterns of coral-dinoflagellate associations in Acropora: Significance of local availability and physiology of Symbiodinium strands and host-symbiont selectivity, Proc. R. Soc. Lond. B, 268, 1759, 10.1098/rspb.2001.1733

Fabricus, 2004, Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories, Mol. Ecol., 13, 2445, 10.1111/j.1365-294X.2004.02230.x

Stimson, 1991, The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen enrichment and control conditions, J. Exp. Mar. Biol. Ecol., 153, 63, 10.1016/S0022-0981(05)80006-1

Curran, 1998, Spatial distribution of DMS and DMSP in the Australasian sector of the Southern Ocean. In: Special Issue on the Southern Hemisphere Marine Aerosol Characterisation Experiment (ACE 1), J. Geophys. Res., 103, 16677, 10.1029/97JD03453

Tapiolas, 2013, Direct measurement of dimethylsulphoniopropionate (DMSP) in reef-building corals using quantitative nuclear magnetic resonance (qNMR) spectroscopy, J. Exp. Mar. Biol. Ecol., 443, 85, 10.1016/j.jembe.2013.02.037

Stimson, 2002, Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality, Coral Reefs, 21, 409, 10.1007/s00338-002-0264-3

Strychar, 2004, Loss of Symbiodinium from bleached Australian scleractinian corals (Acropora hyacinthus, Favites complanata and Porites solida), Mar. Freshw. Res., 55, 135, 10.1071/MF03080

Ralph, 2001, Zooxanthellae expelled from bleached corals at 33 degrees C are photosynthetically competent, Mar. Ecol. Prog. Ser., 220, 163, 10.3354/meps220163

Jones, 2001, Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: Photoprotection, photo-inactivation and the relationship to coral bleaching, Plant Cell Environ., 24, 89, 10.1046/j.1365-3040.2001.00648.x

Andreae, 1990, Ocean-atmosphere interactions in the global biogeochemical sulphur cycle, Mar. Chem., 30, 1, 10.1016/0304-4203(90)90059-L

Heckathorn, 1998, The small, methionine-rich chloroplast heat-shock protein protects photosystem 11 electron transport during heat stress, Plant Physiol., 116, 439, 10.1104/pp.116.1.439

Muslim, 2003, The seasonal variation of dissolved nutrients, chlorophyll a and suspended sediments at Nelly Bay, Magnetic Island, Estuar. Coast. Shelf Sci., 57, 445, 10.1016/S0272-7714(02)00373-6