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Effects of high temperature and CO2 on intracellular DMSP in the cold-water coral Lophelia pertusa

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Abstract

Significant warming and acidification of the oceans is projected to occur by the end of the century. CO2 vents, areas of upwelling and downwelling, and potential leaks from carbon capture and storage facilities may also cause localised environmental changes, enhancing or depressing the effect of global climate change. Cold-water coral ecosystems are threatened by future changes in carbonate chemistry, yet our knowledge of the response of these corals to high temperature and high CO2 conditions is limited. Dimethylsulphoniopropionate (DMSP), and its breakdown product dimethylsulphide (DMS), are putative antioxidants that may be accumulated by invertebrates via their food or symbionts, although recent research suggests that some invertebrates may also be able to synthesise DMSP. This study provides the first information on the impact of high temperature (12 °C) and high CO2 (817 ppm) on intracellular DMSP in the cold-water coral Lophelia pertusa from the Mingulay Reef Complex, Scotland (56°49′N, 07°23′W), where in situ environmental conditions are meditated by tidally induced downwellings. An increase in intracellular DMSP under high CO2 conditions was observed, whilst water column particulate DMS + DMSP was reduced. In both high temperature treatments, intracellular DMSP was similar to the control treatment, whilst dissolved DMSP + DMS was not significantly different between any of the treatments. These results suggest that L. pertusa accumulates DMSP from the surrounding water column; uptake may be up-regulated under high CO2 conditions, but mediated by high temperature. These results provide new insight into the biotic control of deep-sea biogeochemistry and may impact our understanding of the global sulphur cycle, and the survival of cold-water corals under projected global change.

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References

  • Anthony KRN, Kleypas JA, Gattuso J-P (2011) Coral reefs modify their seawater carbon chemistry—implications for impacts of ocean acidification. Glob Change Biol 17:3655–3666. doi:10.1111/j.1365-2486.2011.02510.x

    Article  Google Scholar 

  • Arnold HE, Kerrison P, Steinke M (2012) Interacting effects of ocean acidification and warming on growth and DMS-production in the haptophyte coccolithophore Emiliania huxleyi. Glob Change Biol. doi:10.1111/gcb.12105

    Google Scholar 

  • Avgoustidi V, Nightingale PD, Joint I, Steinke M, Turner S, Hopkins FE, Liss PS (2012) Decreased marine dimethyl sulfide production under elevated CO2 levels in mesocosm and in vitro studies. Environ Chem 9:399–404

    Article  CAS  Google Scholar 

  • Ayers GP, Cainey JM (2007) The CLAW hypothesis: a review of the major developments. Environ Chem 4:366–374. doi:10.1071/EN07080

    Article  CAS  Google Scholar 

  • Blackford J, Jones N, Proctor R, Holt J, Widdicombe S, Lowe D, Rees A (2009) An initial assessment of the potential environmental impact of CO2 escape from marine carbon capture and storage systems. Proc Inst Mech Eng Part A J Power Energy 223:269–280

    Article  Google Scholar 

  • Broadbent AD, Jones GB, Jones RJ (2002) DMSP in corals and benthic algae from the Great Barrier Reef. Estuar Coast Shelf Sci 55:547–555. doi:10.1006/ecss.2002.1021

    Article  CAS  Google Scholar 

  • Burdett HL, Aloisio E, Calosi P, Findlay HS, Widdicombe S, Hatton AD, Kamenos NA (2012) The effect of chronic and acute low pH on the intracellular DMSP production and epithelial cell morphology of red coralline algae. Mar Biol Res 8:756–763

    Article  Google Scholar 

  • Burdett HL, Donohue PJC, Hatton AD, Alwany MA, Kamenos NA (2013) Spatiotemporal variability of Dimethylsulphoniopropionate on a fringing coral reef: the role of reefal carbonate chemistry and environmental variability. PLoS ONE 8:e64651

    Article  CAS  Google Scholar 

  • Burdett HL, Carruthers M, Donohue PJC, Wicks LC, Hennige SJ, Roberts JM, Kamenos NA (2014) Impacts of increased CO2 and temperature upon DMSP production in the cold-water coral, Lophelia pertusa, from short-term experiments carried out on cruise D366/7. British Oceanographic Data Centre, Natural Environment Research Council, UK. doi:10.5285/f1a75a9f-95c9-57c1-e044-000b5de50f38

  • Cairns SD (1994) Scleractina of the temperate North Pacific. Smithsonian contributions to zoology. Smithsonian Institution Press, Washington

    Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04

    Google Scholar 

  • C.B.D. (2008) COP 9 Decision IX/20: Marine and coastal biodiversity

  • Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655–661

    Article  CAS  Google Scholar 

  • Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 1/2H2(g) = Ag(s) + HCl(aq), and and the standard acidity constant of the ion HSO4 − in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127

    Article  CAS  Google Scholar 

  • Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A Oceanogr Res Pap 34:1733–1743

    Article  CAS  Google Scholar 

  • Dodds LA, Roberts JM, Taylor AC, Marubini F (2007) Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change. J Exp Mar Biol Ecol 349:205–214

    Article  CAS  Google Scholar 

  • Davies AJ, Duineveid GCA, Lavaleye MSS, Bergman MJN, van Haren H, Roberts JM (2009) Downwelling and deep-water bottom currents as food supply mechanisms to the cold-water coral Lophelia pertusa (Scleractinia) at the Mingulay Reef complex. Limnol Oceanogr 54:620–629

    Google Scholar 

  • Duarte C, Hendriks I, Moore T, Olsen Y, Steckbauer A, Ramajo L, Carstensen J, Trotter J, McCulloch M (2013) Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuar Coast 36:221–236. doi:10.1007/s12237-013-9594-3

    Article  CAS  Google Scholar 

  • Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320:1490–1492. doi:10.1126/science.1155676

    Article  CAS  Google Scholar 

  • Findlay HS, Artioli Y, Moreno Navas J, Hennige SJ, Wicks LC, Huvenne VAI, Woodward EMS, Roberts JM (2013) Tidal downwelling and implications for the carbon biogeochemistry of cold-water corals in relation to future ocean acidification and warming. Glob Change Biol. doi:10.1111/gcb.12256

    Google Scholar 

  • Form AU, Riebesell U (2012) Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa. Glob Change Biol 18:843–853. doi:10.1111/j.1365-2486.2011.02583.x

    Article  Google Scholar 

  • Fosså JH, Mortensen PB, Furevik DM (2002) The deep-water coral Lophelia pertusa in Norwegian waters: distribution and fishery impacts. Hydrobiologia 471:1–12

    Article  Google Scholar 

  • Green DH, Shenoy DM, Hart MC, Hatton AD (2011) DMS oxidation coupled to biomass production by a marine flavobacterium. Appl Environ Microbiol 77:3137–3140

    Article  CAS  Google Scholar 

  • Gruber N, Hauri C, Lachkar Z, Loher D, Frölicher TL, Plattner G-K (2012) Rapid progression of ocean acidification in the California current system. Science 337:220–223. doi:10.1126/science.1216773

    Article  CAS  Google Scholar 

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99

    Article  CAS  Google Scholar 

  • Hatton A, Shenoy D, Hart M, Mogg A, Green D (2012) Metabolism of DMSP, DMS and DMSO by the cultivable bacterial community associated with the DMSP-producing dinoflagellate Scrippsiella trochoidea. Biogeochemistry 110:131–146. doi:10.1007/s10533-012-9702-7

    Article  CAS  Google Scholar 

  • Hennige SJ, Wicks LC, Kamenos NA, Bakker DCE, Findlay HS, Dumousseaud C, Roberts JM (2014) Short-term metabolic and growth responses of the cold-water coral Lophelia pertusa to ocean acidification. Deep Sea Res Part II: Top Stud Oceanogr 99:27–35. doi:10.1016/j.dsr2.2013.07.005

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Inglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  Google Scholar 

  • Hopkins FE, Turner SM, Nightingale PD, Steinke M, Bakker D, Liss PS (2010) Ocean acidification and marine trace gas emissions. Proc Acad Nat Sci Phila 107:760–765

    Article  CAS  Google Scholar 

  • Huggett M, Williamson J, de Nys R, Kjelleberg S, Steinberg P (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149:604–619. doi:10.1007/s00442-006-0470-8

    Article  Google Scholar 

  • IPCC (2007) Summary for policymakers. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambrdige

    Google Scholar 

  • Kerrison P, Suggett D, Hepburn L, Steinke M (2012) Effect of elevated pCO2 on the production of dimethylsulphoniopropionate (DMSP) and dimethylsulphide (DMS) in two species of Ulva (Chlorophyceae). Biogeochemistry 110:5–16. doi:10.1007/s10533-012-9707-2

    Article  CAS  Google Scholar 

  • Kiene RP, Slezak D (2006) Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling. Limnol Oceanogr Methods 4:80–95

    Article  CAS  Google Scholar 

  • Maier C, Watremez P, Taviani M, Weinbauer MG, Gattuso JP (2012) Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals. Proc R Soc B: Biol Sci 279:1716–1723. doi:10.1098/rspb.2011.1763

    Article  CAS  Google Scholar 

  • McCulloch M, Trotter J, Montagna P, Falter J, Dunbar R, Freiwald A, Försterra G, López Correa M, Maier C, Rüggeberg A, Taviani M (2012) Resilience of cold-water scleractinian corals to ocean acidification: boron isotopic systematics of pH and saturation state up-regulation. Geochim Cosmochim Acta 87:21–34. doi:10.1016/j.gca.2012.03.027

    Article  CAS  Google Scholar 

  • Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907

    Article  CAS  Google Scholar 

  • NOAA (2014) Trends in atmospheric carbon dioxide. http://www.esrl.noaa.gov/gmd/ccgg/trends/mlo.html. Accessed 2 April 2014

  • Pierrot D, Lewis E, Wallace DWR (2006) CO2SYS DOS Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information analysis Center. Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, TN

  • Raina J-B, Tapiolas DM, Foret S, Lutz A, Abrego D, Ceh J, Seneca FO, Clode PL, Bourne DG, Willis BL, Motti CA (2013) DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502:677–680. doi:10.1038/nature12677

    Article  CAS  Google Scholar 

  • Roberts J, participants (2013) Changing oceans expedition 2012. RRS James Cook 073 Cruise Report

  • Roberts JM, Wheeler A, Freiwald A, Cairns SD (2009) Cold-water corals: the biology and geology of deep-sea coral habitats. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Spielmeyer A, Pohnert G (2012) Influence of temperature and elevated carbon dioxide on the production of dimethylsulfoniopropionate and glycine betaine by marine phytoplankton. Mar Environ Res 73:62–69

    CAS  Google Scholar 

  • Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43:183–197

    Article  CAS  Google Scholar 

  • Steller D, Cáceres-Martinez C (2009) Coralline algal rhodoliths enhance larval settlement and early growth of the Pacific calico scallop Argopecten ventricosus. Mar Ecol Prog Ser 396:49–60. doi:10.3354/meps08261

    Article  Google Scholar 

  • Sunda W, Kieber DJ, Kiene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320

    Article  CAS  Google Scholar 

  • Turner SM, Malin G, Bagander LE, Leck C (1990) Interlaboratory calibration and sample analysis of dimethyl sulfide in water. Mar Chem 29:47–62

    Article  CAS  Google Scholar 

  • Van Alstyne K, Puglisi M (2007) DMSP in marine macroalgae and macroinvertebrates: distribution, function, and ecological impacts. Aquat Sci 69:394–402

    Article  Google Scholar 

  • Van Alstyne K, Schupp P, Slattery M (2006) The distribution of dimethylsulfoniopropionate in tropical Pacific coral reef invertebrates. Coral Reefs 25:321–327. doi:10.1007/s00338-006-0114-9

    Article  Google Scholar 

  • Van Alstyne K, Dominique V, Muller-Parker G (2009) Is dimethylsulfoniopropionate (DMSP) produced by the symbionts or the host in an anemone–zooxanthella symbiosis? Coral Reefs 28:167–176

    Article  Google Scholar 

  • Vogt M, Steinke M, Turner S, Paulino A, Meyerhöfer M, Riebesell U, LeQuéré C, Liss P (2008) Dynamics of dimethylsulphoniopropionate and dimethylsulphide under different CO2 concentrations during a mesocosm experiment. Biogeosciences 5:407–419. doi:10.5194/bg-5-407-2008

    Article  CAS  Google Scholar 

  • Wingenter OW, Haase KB, Zeigler M, Blake DR, Sherwood RF, Sive BC, Paulino A, Thyrhaug R, Larsen A, Schulz K, Meyerhofer M, Reibesell U (2007) Unexpected consequences of increasing CO2 and ocean acidity on marine production of DMS and CH2ClI: potential climate impacts. Geophys Res Lett 34:L05710

    Article  Google Scholar 

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Acknowledgments

This paper is a contribution to the UK Ocean Acidification Research Programme (Natural Environment Research Council (NERC) Grant NE/H017305/) and to the Marine Alliance for Science and Technology Scotland (MASTS). This research was conducted whilst HLB was initially in receipt of NERC studentship funding (NE/H525303/1) and ultimately a MASTS Research Fellowship, PJCD was in receipt of a MASTS PhD studentship, NAK was in receipt of Royal Society of Edinburgh/Scottish Government Fellowship (RES 48704/1) and SJH was in receipt of a NERC Independent Research Fellowship (NE/K009028/1). SJH, LCW and JMR acknowledge support from Heriot–Watt University’s Environment and Climate Change Theme. Many thanks extend to the captain and crew of the RRS James Cook (cruise 073) for assistance at sea. The data from this study are freely available from the British Oceanographic Data Centre (Burdett et al. 2014).

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Authors and Affiliations

  1. Scottish Oceans Institute, University of St Andrews, St Andrews, KY16 8LB, UK

    H. L. Burdett

  2. Department of Earth and Environmental Sciences, University of St Andrews, St Andrews, KY16 9AJ, UK

    H. L. Burdett

  3. School of Geographical and Earth Sciences, University of Glasgow, Glasgow, G12 8QQ, UK

    H. L. Burdett, P. J. C. Donohue & N. A. Kamenos

  4. School of Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK

    M. Carruthers & N. A. Kamenos

  5. Centre for Marine Biodiversity and Biotechnology, Heriot-Watt University, Edinburgh, EH14 4AS, UK

    L. C. Wicks, S. J. Hennige & J. M. Roberts

  6. Scottish Association for Marine Science, Oban, PA37 1QA, UK

    J. M. Roberts

  7. Center for Marine Science, University of North Carolina Wilmington, 601 S. College Road, Wilmington, NC, 28403-5928, USA

    J. M. Roberts

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  1. H. L. Burdett
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  2. M. Carruthers
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Correspondence to H. L. Burdett.

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Communicated by H. Pörtner.

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Burdett, H.L., Carruthers, M., Donohue, P.J.C. et al. Effects of high temperature and CO2 on intracellular DMSP in the cold-water coral Lophelia pertusa . Mar Biol 161, 1499–1506 (2014). https://doi.org/10.1007/s00227-014-2435-5

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