Skip to main content

Advertisement

SpringerLink
Log in

Molecular mechanisms underlying the physiological responses of the cold-water coral Desmophyllum dianthus to ocean acidification

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Cold-water corals (CWCs) are thought to be particularly vulnerable to ocean acidification (OA) due to increased atmospheric pCO2, because they inhabit deep and cold waters where the aragonite saturation state is naturally low. Several recent studies have evaluated the impact of OA on organism-level physiological processes such as calcification and respiration. However, no studies to date have looked at the impact at the molecular level of gene expression. Here, we report results of a long-term, 8-month experiment to compare the physiological responses of the CWC Desmophyllum dianthus to OA at both the organismal and gene expression levels under two pCO2/pH treatments: ambient pCO2 (460 μatm, pHT = 8.01) and elevated pCO2 (997 μatm, pHT = 7.70). At the organismal level, no significant differences were detected in the calcification and respiration rates of D. dianthus. Conversely, significant differences were recorded in gene expression profiles, which showed an up-regulation of genes involved in cellular stress (HSP70) and immune defence (mannose-binding c-type lectin). Expression of alpha-carbonic anhydrase, a key enzyme involved in the synthesis of coral skeleton, was also significantly up-regulated in corals under elevated pCO2, indicating that D. dianthus was under physiological reconditioning to calcify under these conditions. Thus, gene expression profiles revealed physiological impacts that were not evident at the organismal level. Consequently, understanding the molecular mechanisms behind the physiological processes involved in a coral’s response to elevated pCO2 is critical to assess the ability of CWCs to acclimate or adapt to future OA conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Allemand D, Tambutté E, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition Springer, New York, pp 119–150

    Chapter  Google Scholar 

  • Allemand D, Ferrier-Pagés C, Furla P, Houlbréque F, Puverel S, Reynaud S, Tambutté É, Tambutté S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. C R Palevol 3:453–467

    Article  Google Scholar 

  • Anagnostou E, Huang KF, You CF, Sikes E, Sherrell R (2012) Evaluation of boron isotope ratio as a pH proxy in the deep sea coral Desmophyllum dianthus: Evidence of physiological pH adjustment. Earth Planet Sci Lett 349:251–260

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Braga-Henriques A, Porteiro FM, Ribeiro PA, de Matos V, Sampaio Í, Ocaña O, Santos RS (2013) Diversity, distribution and spatial structure of the cold-water coral fauna of the Azores (NE Atlantic). Biogeosciences 10:529–590

    Article  Google Scholar 

  • Bucher DJ, Harriott VJ, Roberts LG (1998) Skeletal micro-density, porosity and bulk density of acroporid corals. J Exp Mar Biol Ecol 228:117–136

    Article  Google Scholar 

  • Buddemeier RW, Kinzie RA (1976) Coral growth. Oceanogr Mar Biol Annu Rev 14:183–222

    Google Scholar 

  • Cairns SD, Zibrowius H (1997) Cnidaria Anthozoa: Azooxanthellate Scleractinia from the Philippine and Indonesian regions. Mem Mus Natl Hist Nat 172:27–243

    Google Scholar 

  • Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395

    Article  Google Scholar 

  • De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcification on the Great Barrier Reef. Science 323:116–119

    Article  PubMed  Google Scholar 

  • DeSalvo MK, Sunagawa S, Voolstra CR, Medina M (2010) Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar Ecol Prog Ser 402:97–111

    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 I 34:1733–1743

    Article  CAS  Google Scholar 

  • Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192

    Article  Google Scholar 

  • Evans TG, Hofmann GE (2012) Defining the limits of physiological plasticity: how gene expression can assess and predict the consequences of ocean change. Philos Trans R Soc Lond B 367:1733–1745

    Article  Google Scholar 

  • Fabricius KE, Langdon C, Uthicke S, Humphrey CH, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Climate Change 1:165–169

    Article  CAS  Google Scholar 

  • Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366

    Article  CAS  PubMed  Google Scholar 

  • Findlay HS, Wood HL, Kendall MA, Spicer JI, Twitchett R, Widdicombe S (2011) Comparing the impact of high CO2 on calcium carbonate structures in different marine organisms. Mar Biol Res 7:565–575

    Article  Google Scholar 

  • Form AU, Riebesell U (2012) Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa. Global Change Biol 18:843–853

    Article  Google Scholar 

  • Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43

    Google Scholar 

  • Gattuso J-P, Frankignoulle M, Bourge I, Romaine S, Buddemeier RW (1998) Effect of calcium carbonate saturation of seawater on coral calcification. Global Planet Change 18:37–46

    Article  Google Scholar 

  • Gori A, Grover R, Orejas C, Sikorski S, Ferrier-Pagès C (2013) Uptake of dissolved free amino acids by four cold-water coral species from the Mediterranean Sea. Deep-Sea Res Part II (doi:10.1016/j.dsr2.2013.06.007)

  • Grasshoff K (1976) Methods of seawater analysis. Verlag Chemie, New York

    Google Scholar 

  • Guinotte JM, Orr J, Cairns S, Freiwald A, Morgan L, Robert G (2006) Will human-induced changes in seawater chemistry alter the distribution of deep-sea scleractinian corals? Front Ecol Environ 4:141–146

    Article  Google Scholar 

  • Hamel JF, Sun Z, Mercier A (2010) Influence of size and seasonal factors on the growth of the deep-sea coral Flabellum alabastrum in mesocosm. Coral Reefs 29:521–525

    Article  Google Scholar 

  • Hennige SJ, Wicks L, Kamenos N, Bakker D, Findlay H, Dumousseaud C, Roberts M (2013) Short-term metabolic and growth responses of the cold-water coral Lophelia pertusa to ocean acidification. Deep-Sea Res Part II (doi: 10.1016/j.dsr2.2013.07.005)

  • Holcomb M, Cohen AL, McCorkle DC (2012) An investigation of the calcification response of the scleractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender. Biogeosciences 9:29–39

    Article  CAS  Google Scholar 

  • IPCC (2007) Climate change 2007: the physical science basis. Cambridge University Press, United Kingdom

    Google Scholar 

  • Kaniewska P, Campbell PR, Kline DI, Rodriguez- Lanetty M, Miller DJ, Dove S, Hoegh-Guldberg O (2012) Major Cellular and Physiological Impacts of Ocean Acidification on a Reef Building Coral. PLoS ONE 7(4):e34659

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kültz D (2003) Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J Exp Biol 206:3119–3124

    Article  PubMed  Google Scholar 

  • Kvennefors ECE, Leggat W, Hoegh-Guldberg O, Degnan BM, Barnes AC (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 32:1582–1592

    Article  CAS  PubMed  Google Scholar 

  • Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res C 110:C09S07

    Google Scholar 

  • Lewis E, Wallace DWR (1998) 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. (http://pubs.usgs.gov/of/2010/1280/pdf/ofr_2010-1280.pdf)

  • Maier C, Watremez M, Taviani M, Weinbauer G, Gattuso JP (2012) Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals. Proc R Soc, B 279:1716–1723

    Article  CAS  Google Scholar 

  • Maier C, Kluijver AD, Agis M, Brussaard CPD, van Duyl FC, Weinbauer MG (2011) Dynamics of nutrients, total organic carbon, prokaryotes and viruses in onboard incubations of cold-water corals. Biogeosciences 8:2609–2620

    Article  CAS  Google Scholar 

  • Maier C, Schubert A, Berzunza Sànchez MM, Weinbauer MG, Watremez P, Gattuso J-P (2013a) End of the century pCO2 levels do not impact calcification in Mediterranean cold-water corals. PLoS ONE 8(4):e62655

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maier C, Bils F, Weinbauer MG, Watremez P, Peck MA, Gattuso J-P (2013b) Respiration of Mediterranean cold-water corals is not affected by ocean acidification as projected for the end of the century. Biogeosciences 10:5671–5680

    Article  Google Scholar 

  • McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42:95–117

    Article  CAS  Google Scholar 

  • McCulloch M, Falter J, Trotter J, Montagna P (2012a) Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Climate Change 2:623–627

    Article  CAS  Google Scholar 

  • McCulloch M, Trotter J, Montagna P, Falter J, Dunbar R, Freiwald A, Fosterra G, Lopez-Correa M, Maier C, Ruggeberg A, Taviani M (2012b) 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mortensen PB (2001) Aquarium observations on the deep-water coral Lophelia pertusa (L., 1758) (Scleractinia) and selected associated invertebrates. Ophelia 54:83–104

    Article  Google Scholar 

  • Moya A, Tambutté S, Bertucci A, Tambutté É, Lotto S, Vullo D, Supuran CT, Allemand D, Zoccola D (2008) Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization. J Biol Chem 283:25475–25484

    Article  CAS  PubMed  Google Scholar 

  • Moya A, Huisman L, Ball EE, Hayward DC, Grasso LC, Chua CM, Woo HN, Gattuso J-P, Forêt S, Miller DJ (2012) Whole transcriptome analysis of the coral Acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification. Mol Ecol 21:2440–2454

    Article  CAS  PubMed  Google Scholar 

  • Mydlarz LD, Holthouse SF, Peters EC, Harvell CD (2008) Cellular Responses in Sea Fan Corals: Granular Amoebocytes React to Pathogen and Climate Stressors. PLoS ONE 3(3):e1811

    Article  PubMed Central  PubMed  Google Scholar 

  • Naumann MS, Orejas C, Wild C, Ferrier-Pagès C (2011) First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold-water coral. J Exp Biol 214:3570–3576

    Article  CAS  PubMed  Google Scholar 

  • Naumann MS, Niggl W, Laforsch C, Glaser C, Wild C (2009) Coral surface area quantification - evaluation of established methods by comparison with computer tomography. Coral Reefs 28:109–117

    Article  Google Scholar 

  • Orejas C, Ferrier-Pages C, Reynaud S, Gori A, Beraud E, Tsounis G, Allemand D, Gili J (2011) Long-term growth rates for Mediterranean cold-water coral species maintained in aquaria. Mar Ecol Prog Ser 429:57–65

    Article  Google Scholar 

  • Orr JC (2011) Recent and future changes in ocean carbonate chemistry. In: Gattuso J-P, Hansson L (eds) Ocean Acidification. Oxford University Press, Oxford, pp 41–66

    Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  CAS  PubMed  Google Scholar 

  • Pelejero C, Calvo E, Hoegh-Guldberg O (2010) Paleo-perspective on ocean acidification. Trends Ecol Evol 25:332–345

    Article  PubMed  Google Scholar 

  • Ries JB, Cohen AL, McKorkle DC (2009) Marine calcifers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134

    Article  CAS  Google Scholar 

  • Ries JB, Cohen AI, McCorkle DC (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674

    Article  Google Scholar 

  • Rodolfo-Metalpa R, Martin S, Ferrier-Pages C, Gattuso JP (2010) Response of the temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences 7:289–300

    Article  CAS  Google Scholar 

  • Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso J-P, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change 1:308–312

    Article  CAS  Google Scholar 

  • SAS Institute (2004) User’s manual, version 9.0. SAS Institute Cary, NC

  • Sorenson JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037

    Article  Google Scholar 

  • Trotter J, Montagna P, McCulloch M, Silenzif S, Reynaud S, Mortimerh G, Martini S, Ferrier-Pagés C, Gattuso J-P, Rodolfo-Metalpa R (2011) Quantifying the pH ‘vital effect’ in the temperate zooxanthellate coral Cladocora caespitosa: validation of the boron seawater pH proxy. Earth Planet Sci Lett 303:163–173

    Article  CAS  Google Scholar 

  • van Duyl FC, Hegeman J, Hoogstraten A, Maier C (2008) Dissolved carbon fixation by sponge-microbe consortia of deep water coral mounds in the NE Atlantic Ocean. Mar Ecol Prog Ser 358:137–150

    Article  Google Scholar 

  • Vidal-Dupiol J, Zoccola D, Tambutté É, Grunau C, Cosseau C (2013) Genes Related to Ion-Transport and Energy Production Are Upregulated in Response to CO2-Driven pH Decrease in Corals: New Insights from Transcriptome Analysis. PLoS ONE 8(3):e58652

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vidal-Dupiol J, Ladrière O, Meistertzheim AL, Fouré L, Adjeroud M, Mitta G (2011) Physiological responses of the scleractinian coral Pocillopora damicornis to bacterial stress from Vibrio coralliilyticus. J Exp Biol 214:1533–1545

    Article  CAS  PubMed  Google Scholar 

  • Vidal-Dupiol J, Adjeroud M, Roger E, Foure L, Duval D, Mone Y, Mitta G (2009) Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BMC Physiol 9(1):14

    Article  PubMed Central  PubMed  Google Scholar 

  • Ward JR, Kim K, Harvell CD (2007) Temperature drives coral disease resistance and pathogen virulence. Mar Ecol Prog Ser 329:115–121

    Article  Google Scholar 

  • Wicks LC, Roberts JM (2012) Benthic invertebrates in a high CO2 world. Oceanogr Mar Biol Annu Rev 50:127–188

    Google Scholar 

  • Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at a cost. Proc R Soc, B 275:1767–1773

    Article  Google Scholar 

  • Zoccola D, Tambuttè É, Kulhanek E, Puverel S, Scimeca J-C, Allemand D, Tambuttè S (2004) Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. Biochim Biophys Acta 1663:117–126

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Emmanuelle Maitre, Andreia Braga-Henriques, and Luis Pires for assistance in aquaria maintenance. IMAR-DOP/UAz is a Research and Development Unit no. 531 and LARSyS-Associated Laboratory no.9 funded by the Portuguese Foundation for Science and Technology (FCT) through FCT project Pest/OE/EEI/LA0009/2011-2014 & COMPETE/QREN and by the Azores Fund for Science and Technology (FRCT). This study was supported by the European Community’s Seventh Framework Programme (FP7/2007–2013) through a Marie-Curie IRG Fellowship to MC-S (CoralChange, project no. 231109) and project HERMIONE (grant agreement no. 226354). Coral specimens used in this study were obtained by the observer onboard programme financed by CoralFISH project (grant agreement no. 213144). MC-S was supported by an FCT post-doctoral grant (SFRH/BPD/34634/2007). TC was supported by the doctoral grant from the Regional Directorate for Science, Technology and Communications (DRCTC), Regional Government of the Azores (M3.1.2/F/052/2011). RB was supported by FCT′s “Ciência 2007” (OE/COMPETE) recruitment programme.

Author information

Authors and Affiliations

  1. LARSyS Associated Laboratory, Department of Oceanography and Fisheries (DOP), Centre of IMAR of the University of the Azores, Rua Prof. Dr. Frederico Machado 4, 9901-862, Horta, Portugal

    M. Carreiro-Silva, T. Cerqueira, A. Godinho, R. S. Santos & R. Bettencourt

  2. IPMA – Portuguese Institute of Sea and Atmosphere, Av. Brasília, 1449-006, Lisbon, Portugal

    M. Caetano

Authors
  1. M. Carreiro-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. Cerqueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Godinho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Caetano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. S. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. Bettencourt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Carreiro-Silva.

Additional information

Communicated by Biology Editor Anastazia Banaszak

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 29 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carreiro-Silva, M., Cerqueira, T., Godinho, A. et al. Molecular mechanisms underlying the physiological responses of the cold-water coral Desmophyllum dianthus to ocean acidification. Coral Reefs 33, 465–476 (2014). https://doi.org/10.1007/s00338-014-1129-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-014-1129-2

Keywords

Search

Navigation