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Patterns of Gene Expression in a Scleractinian Coral Undergoing Natural Bleaching

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Abstract

Coral bleaching is a major threat to coral reefs worldwide and is predicted to intensify with increasing global temperature. This study represents the first investigation of gene expression in an Indo-Pacific coral species undergoing natural bleaching which involved the loss of algal symbionts. Quantitative real-time polymerase chain reaction experiments were conducted to select and evaluate coral internal control genes (ICGs), and to investigate selected coral genes of interest (GOIs) for changes in gene expression in nine colonies of the scleractinian coral Acropora millepora undergoing bleaching at Magnetic Island, Great Barrier Reef, Australia. Among the six ICGs tested, glyceraldehyde 3-phosphate dehydrogenase and the ribosomal protein genes S7 and L9 exhibited the most constant expression levels between samples from healthy-looking colonies and samples from the same colonies when severely bleached a year later. These ICGs were therefore utilised for normalisation of expression data for seven selected GOIs. Of the seven GOIs, homologues of catalase, C-type lectin and chromoprotein genes were significantly up-regulated as a result of bleaching by factors of 1.81, 1.46 and 1.61 (linear mixed models analysis of variance, P < 0.05), respectively. We present these genes as potential coral bleaching response genes. In contrast, three genes, including one putative ICG, showed highly variable levels of expression between coral colonies. Potential variation in microhabitat, gene function unrelated to the stress response and individualised stress responses may influence such differences between colonies and need to be better understood when designing and interpreting future studies of gene expression in natural coral populations.

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References

  • Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, Beltran-Ramirez V, Miller DJ, Wiedenmann J, Salih A, Matz MV (2008) Diversity and evolution of coral fluorescent proteins. PLoS ONE 3:e2680

    Article  PubMed  Google Scholar 

  • Bates BC, Kundzewicz ZW, Wu S, Palutikof JP (eds) (2008) Climate Change and Water. Technical Paper of the Intergovernmental Panel on Climate Change, IPCC Secretariat, Geneva: pp 210

  • Bay LK, Nielsen HB, Jarmer H, Seneca FO, van Oppen MJ (2009a) Transcriptomic variation in a coral reveals pathways of clonal organisation. Marine Genomics 2:119–125

    Google Scholar 

  • Bay LK, Ulstrup KE, Nielsen HB, Jarmer H, Goffard N, Willis BL, Miller DJ, van Oppen MJH (2009b) Microarray analysis reveals transcriptional plasticity in the reef building coral Acropora millepora. Mol Ecol 18:3062–3075

    Article  CAS  PubMed  Google Scholar 

  • Beltran-Ramirez V (2008) Molecular aspects of the coral–algal symbiosis. Thesis, James Cook University, Townsville, Australia

  • Berkelmans R, Willis BL (1999) Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18:219–228

    Article  Google Scholar 

  • Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions. Coral Reefs 23:74–83

    Article  Google Scholar 

  • Boldt L, Yellowlees D, Dove S, Leggat B (2009) The effect of fluctuating light on Symbiodinium photosynthetic gene expression. Abstracts of 11th International Coral Reef Symposium, Fort Lauderdale, Florida, USA. July 7–July 11, 2008, p 29

  • Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta (G) 1760:1690–1695

    CAS  Google Scholar 

  • Bourne D, Iida Y, Uthicke S, Smith-Keune C (2008) Changes in coral-associated microbial communities during a bleaching event. ISME J 2:350–363

    Article  CAS  PubMed  Google Scholar 

  • Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Article  Google Scholar 

  • Brown BE, Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar Biol 122:655–663

    Article  Google Scholar 

  • Brown BE, Downs CA, Dunne RP, Gibb SW (2002) Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar Ecol Prog Ser 242:119–129

    Article  Google Scholar 

  • Bustin S (2004) Quantification of nucleic acids by PCR. In: A–Z of quantitative PCR, Vol. International University Line, La Jolla, CA, USA

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  PubMed  Google Scholar 

  • Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144

    Article  Google Scholar 

  • Császár NBM, Seneca FO, van Oppen MJ (2009) Variation in expression levels of antioxidant genes in the scleractinian coral Acropora millepora under laboratory thermal stress conditions. Mar Ecol Prog Ser 392:93–102

    Google Scholar 

  • Demidenko E (2004) Mixed models, theory and application, Wiley-Interscience, Hoboken

    Book  Google Scholar 

  • Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952–3971

    Article  CAS  PubMed  Google Scholar 

  • Dove S (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar Ecol Prog Ser 272:99–116

    Article  Google Scholar 

  • Dove S, Takabayashi M, Hoegh-Guldberg O (1995) Isolation and partial characterization of the pink and blue pigments of Pocilloporid and Acroporid corals. Biol Bull 189:288–297

    Article  CAS  Google Scholar 

  • Dove SG, Hoegh-Guldberg O, Ranganathan S (2001) Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19:197–204

    Article  Google Scholar 

  • Dove S, Ortiz JC, Enriquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Oceanogr 51:1149–1158

    Article  Google Scholar 

  • Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543

    Article  CAS  PubMed  Google Scholar 

  • Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53

    Article  Google Scholar 

  • Dykens JA, Shick M (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297:579–580

    Article  CAS  Google Scholar 

  • Edge SE, Morgan MB, Gleason DF, Snell TW (2005) Development of a coral cDNA array to examine gene expression profiles in Montastraea faveolata exposed to environmental stress. Mar Pollut Bull 51:507–523

    Article  CAS  PubMed  Google Scholar 

  • Edge SE, Morgan MB, Snell TW (2008) Temporal analysis of gene expression in a field population of the Scleractinian coral Montastraea faveolata. J Exp Mar Biol Ecol 355:114–124

    Article  CAS  Google Scholar 

  • Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65

    Article  Google Scholar 

  • Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130

    Article  Google Scholar 

  • Gilmore AM, Larkum AWD, Salih A, Itoh S, Shibata Y, Bena C, Yamasaki H, Papina M, van Woesik R (2003) Simultaneous time resolution of the emission spectra of fluorescent proteins and zooxanthellar chlorophyll in reef-building corals. Photochem Photobiol 77:515–523

    Article  CAS  PubMed  Google Scholar 

  • Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17

    Article  Google Scholar 

  • Grasso L, Maindonald J, Rudd S, Hayward D, Saint R, Miller D, Ball E (2008) Microarray analysis identifies candidate genes for key roles in coral development. BMC Genomics 9:540

    Article  PubMed  Google Scholar 

  • Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Natl Acad Sci U S A 103:14288–14293

    Article  CAS  PubMed  Google Scholar 

  • Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19

    Article  PubMed  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci U S A 89:10302–10305

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey SW, Haxo FT (1968) Photosynthetic pigments of symbiotic dinoflagellates (zooxanthellae) from corals and clams. Biol Bull 135:149–165

    Article  CAS  Google Scholar 

  • Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162

    Article  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230

    Article  CAS  Google Scholar 

  • Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc Roy Soc Lond B Biol Sci 275:1359–1365

    Article  CAS  Google Scholar 

  • Kawaguti S (1944) On the physiology of reef corals. VI. Study on the pigments. Palao Tropical Biology Station 2:616–673

    Google Scholar 

  • Kiss-Toth E, Bagstaff SM, Sung HY, Jozsa V, Dempsey C, Caunt JC, Oxley KM, Wyllie DH, Polgar T, Harte M, O’Neill LAJ, Qwarnstrom EE, Dower SK (2004) Human tribbles, a protein family controlling mitogen-activated protein kinase cascades. J Biol Chem 279:42703–42708

    Article  CAS  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 

  • Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283

    Article  CAS  Google Scholar 

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253

    Article  CAS  PubMed  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 

  • Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232

    Article  Google Scholar 

  • Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, Hoegh-Guldberg O (2007) Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318:467–470

    Article  CAS  PubMed  Google Scholar 

  • Matta JL, Trench RK (1991) The enzymatic response of the symbiotic dinoflagellate Symbiodinium microadriaticum (Freudenthal) to growth in vitro under varied oxygen tensions. Symbiosis 11:31–45

    CAS  Google Scholar 

  • Mayfield AB, Gates RD (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp Biochem Physiol Mol Integr Physiol 147:1–10

    Article  Google Scholar 

  • Mayfield AB, Hirst MB, Gates RD (2009) Gene expression normalization in a dual-compartment system: a real-time quantitative polymerase chain reaction protocol for symbiotic anthozoans. Mol Ecol Resour 9:462–470

    Article  Google Scholar 

  • Maynard J, Baird A, Pratchett M (2008) Revisiting the Cassandra syndrome; the changing climate of coral reef research. Coral Reefs 27:745–749

    Article  Google Scholar 

  • Mazel CH (1995) Spectral measurements of fluorescence emission in Caribbean cnidarians. Mar Ecol Prog Ser 120:185–191

    Article  Google Scholar 

  • Mazel CH, Lesser MP, Gorbunov MY, Barry TM, Farrell JH, Wyman KD, Falkowski PG (2003) Green-fluorescent proteins in Caribbean corals. Limnol Oceanogr 48:402–411

    Article  CAS  Google Scholar 

  • Merle P-L, Sabourault C, Richier S, Allemand D, Furla P (2007) Catalase characterization and implication in bleaching of a symbiotic sea anemone. Free Radic Biol Med 42:236–246

    Article  CAS  PubMed  Google Scholar 

  • Meyer E, Aglyamova G, Wang S, Buchanan-Carter J, Abrego D, Colbourne J, Willis B, Matz M (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GS-Flx. BMC Genomics 10:219

    Article  PubMed  Google Scholar 

  • Miyawaki A (2002) Green fluorescent protein-like proteins in reef anthozoa animals. Cell Struct Funct 27:343–347

    Article  CAS  PubMed  Google Scholar 

  • Mladenka P, Simunek T, Hubl M, Hrdina R (2006) The role of reactive oxygen and nitrogen species in cellular iron metabolism. Free Radic Res 40:263–272

    Article  CAS  PubMed  Google Scholar 

  • Morgan MB, Edge SE, Snell TW (2005) Profiling differential gene expression of corals along a transect of waters adjacent to the Bermuda municipal dump. Mar Pollut Bull 51:524–533

    Article  CAS  PubMed  Google Scholar 

  • Moya A, Tambutté S, Béranger G, Gaume B, Scimeca J-C, Allemand D, Zoccola D (2008) Cloning and use of a coral 36B4 gene to study the differential expression of coral genes between light and dark conditions. Mar Biotechnol 10:653–663

    Article  CAS  PubMed  Google Scholar 

  • Muller E, Rogers C, Spitzack A, van Woesik R (2008) Bleaching increases likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John, US Virgin Islands. Coral Reefs 27:191–195

    Article  Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Article  Google Scholar 

  • Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgen, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:445–456

    Article  Google Scholar 

  • Podesta GP, Glynn PW (2001) The 1997–98 El Nino event in Panama and Galapagos: an update of thermal stress indices relative to coral bleaching. Bull Mar Sci 69:43–59

    Google Scholar 

  • R_Development_Core_Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rebrikov D, Trofimov D (2006) Real-time PCR: a review of approaches to data analysis. Appl Biochem Microbiol 42:455–463

    Article  CAS  Google Scholar 

  • Richier S, Merle P-L, Furla P, Pigozzi D, Sola F, Allemand D (2003) Characterization of superoxide dismutases in anoxia- and hyperoxia-tolerant symbiotic cnidarians. Biochim Biophys Acta (G) 1621:84–91

    CAS  Google Scholar 

  • Rodriguez-Lanetty M, Phillips WS, Dove S, Hoegh-Guldberg O, Weis VM (2008) Analytical approach for selecting normalizing genes from a cDNA microarray platform to be used in q-RT-PCR assays: a cnidarian case study. J Biochem Biophys Methods 70:985–991

    Article  CAS  PubMed  Google Scholar 

  • Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269

    Article  CAS  PubMed  Google Scholar 

  • Salih A, Larkum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853

    Article  CAS  PubMed  Google Scholar 

  • Schlichter D, Fricke HW (1990) Coral host improves photosynthesis of endosymbiotic algae. Naturwissenschaften 77:447–450

    Article  Google Scholar 

  • Shigeta M, Sanzen N, Ozawa M, Gu J, Hasegawa H, Sekiguchi K (2003) CD151 regulates epithelial cell–cell adhesion through PKC- and Cdc42-dependent actin cytoskeletal reorganization. J Cell Biol 163:165–176

    Article  CAS  PubMed  Google Scholar 

  • Smith C (2005) The role of genetic and environmental variation on thermal tolerance of a reef-building coral, Acropora millepora. Thesis, University of Queensland, Brisbane, Australia

  • Smith-Keune C, Dove S (2008) Gene expression of a green fluorescent protein homolog as a host-specific biomarker of heat stress within a reef-building coral. Mar Biotechnol 10:166–180

    Article  CAS  PubMed  Google Scholar 

  • Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biol 11:1–11

    Article  Google Scholar 

  • Sunagawa S, Wilson E, Thaler M, Smith M, Caruso C, Pringle J, Weis V, Medina M, Schwarz J (2009) Generation and analysis of transcriptomic resources for a model system on the rise: the sea anemone Aiptasia pallida and its dinoflagellate endosymbiont. BMC Genomics 10:258

    Article  PubMed  Google Scholar 

  • Tchernov D, Gorbunov MY, de Vargas C, Narayan Yadav S, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101:13531–13535

    Article  CAS  PubMed  Google Scholar 

  • Technau U, Rudd S, Maxwell P, Gordon PM, Saina M, Grasso LC, Hayward DC, Sensen CW, Saint R, Holstein TW, Ball EE, Miller DJ (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21:633–639

    Article  CAS  PubMed  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1–11

    Article  Google Scholar 

  • van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883

    Article  PubMed  Google Scholar 

  • Vidal-Dupiol J, Adjeroud M, Roger E, Foure L, Duval D, Mone Y, Ferrier-Pages C, Tambutte E, Tambutte S, Zoccola D, Allemand D, Mitta G (2009) Coral bleaching under thermal stress: putative involvement of host/symbiont recognition mechanisms. BMC Physiology 9:14

    Article  PubMed  Google Scholar 

  • Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK, Szmant AM, Coffroth MA, Medina M (2009) The host transcriptome remains unaltered during the establishment of coral–algal symbioses. Mol Ecol 18:1823–1833

    Article  CAS  PubMed  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96:8007–8012

    Article  CAS  PubMed  Google Scholar 

  • Whanger PD (2000) Selenoprotein W: a review. Cell Mol Life Sci 57:1846–1852

    Article  CAS  PubMed  Google Scholar 

  • Wiedenmann J, Ivanchenko S, Oswald F, Nienhaus GU (2004) Identification of GFP-like proteins in nonbioluminescent, azooxanthellate anthozoa opens new perspectives for bioprospecting. Mar Biotechnol 6:270–277

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Madeleine J. H. van Oppen.

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Table S1

Primers used for the genes under investigation in the qPCR experiment. The best Tblastx match and E value are shown for the EST sequence corresponding to the indicated accession number. The Symbiodinium-specific PCNA primers were designed on the same sequences used in Boldt et al. (2009) (JPEG 428 kb)

Table S1

High resolution image (EPS 601 kb)

Table S2

Ranking of the candidate ICGs according to their M and CV values (Hellemans et al. 2007) calculated between healthy-looking and severely bleached samples across the nine colonies used in qPCR experiment (JPEG 97 kb)

Table S2

High resolution image (EPS 313 kb)

Table S3

The Minimum Information for Publication of Quantitative Real-Time PCR Experiments (MIQE) checklist for reviewers and editors (Bustin et al. 2009) (PDF 1669 kb)

Figure S1

Consistent difference between average quantification cycles of healthy (dark grey) and bleached (light grey) samples in nine colonies, for the best performing ICGs: GAPDH, rpL9 and S7 (JPEG 505 kb)

Figure S1

High resolution image (EPS 418 kb)

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Seneca, F.O., Forêt, S., Ball, E.E. et al. Patterns of Gene Expression in a Scleractinian Coral Undergoing Natural Bleaching. Mar Biotechnol 12, 594–604 (2010). https://doi.org/10.1007/s10126-009-9247-5

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