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Is citrate synthase an energy biomarker in Southwestern Atlantic corals? A comparative, biochemical approach under a simulated scenario of climate change

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Abstract

The Southwestern Atlantic (SWA) corals are more tolerant to global warming than those from the Caribbean Sea, possibly due to their higher heterotrophy and flexibility of symbiotic associations in nutrient-rich waters. Increased heterotrophy promotes greater energy gain via increased mitochondrial respiration, which can be used to face unfavorable conditions. Citrate synthase (CS) is a pacemaker enzyme of cellular respiration, and its activity can be used as a proxy for maximum aerobic capacity, thus being a potential predictor of organism tolerance against climate change. Therefore, we hypothesized that endemic coral species from SWA would have higher CS activity than those of pan-Caribbean distribution after exposure to a simulated scenario of moderate climate change (seawater temperature increase: + 2.5 °C; seawater acidification: − 0.3 pH unit), according to IPCC. Seven species of scleractinian corals and one hydrocoral species were biochemically evaluated in a phylogenetic perspective. Favia gravida, Mussismilia harttii, Montastraea cavernosa, Porites astreoides and Siderastrea stellata were unresponsive regarding CS activity, whereas Millepora alcicornis, Mussismilia hispida and Porites branneri showed a compensatory effect. Regardless of their phylogenetic relationships, endemic SWA coral species revealed higher CS activity than those of pan-Caribbean distribution. We suggest that the unique evolutionary history of SWA endemic species contributes to their biochemical tolerance to climate change, thus supporting the hypothesis of SWA as a refuge for reef life. Although CS is not a suitable biomarker for assessing the putative effects of climate change owing to its species-specific responses, it is an informative metric to indicate stress tolerance of species with different biogeographic origins. This idea becomes particularly evident for SWA reefs, where such a comparative, biochemical approach highlights the greater tolerance of endemic species at the subcellular level of organization.

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References

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

    Article  Google Scholar 

  • Aronson R, Bruckner A, Moore J, Precht B, Weil E (2008) Porites branneri. The IUCN Red List Threatened Species 2008: e.T132921A3494120

  • Banha TNS, Capel KCC, Kitahara MV, Francini-Filho RB, Francini CLB, Sumida PYG, Mies M (2019) Low coral mortality during the most intense bleaching event ever recorded in subtropical Southwestern Atlantic reefs. Coral Reefs 39:515–521

    Article  Google Scholar 

  • Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    PubMed  Google Scholar 

  • Camp M, Shein KA, Foster K and Hendee JC (2016) Does body type really matter? Relating climate change, coral morphology and resiliency. In: American Geophysical Union, Ocean Sciences Meeting

  • Castro CB, Pires DO (2001) Brazilian coral reefs: what we already know and what is still missing. Bull Mar Sci 69:357–371

    Google Scholar 

  • Cohen AL, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127

    Article  Google Scholar 

  • Collins CL, Burnett NP, Ramsey MJ, Wagner K, Zippay ML (2020) Physiological responses to heat stress in an invasive mussel Mytilus galloprovincialis depend on tidal habitat. Marine Environ Res 154:104849

    Article  CAS  Google Scholar 

  • Costa CF, Sassi R, Gorlach-Lira K (2008) Zooxanthellae genotypes in the coral Siderastrea stellata from coastal reefs in Northeastern Brazil. J Exp Mar Biol Ecol 367:149–152

    Article  Google Scholar 

  • Curd A, Pernet F, Corporeau C, Delisle L, Firth LB, Nunes FL, Dubois SF (2019) Connecting organic to mineral: How the physiological state of an ecosystem-engineer is linked to its habitat structure. Ecol Ind 98:49–60

    Article  CAS  Google Scholar 

  • Dahlhoff EP, Stillman JH, Menge BA (2002) Physiological community ecology: variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients. Integr Comp Biol 42:862–871

    Article  PubMed  Google Scholar 

  • Duarte GA, Villela HD, Deocleciano M, Silva D, Barno A, Cardoso PM, Santoro EP (2020) Heat waves are a major threat to turbid coral reefs in Brazil. Front Mar Sci 7:179

    Article  Google Scholar 

  • Duarte G, Calderon EN, Pereira CM, Marangoni LF, Santos HF, Peixoto RS, Castro CB (2015) A novel marine mesocosm facility to study global warming, water quality, and ocean acidification. Ecol Evol 5:4555–4566

    Article  PubMed  PubMed Central  Google Scholar 

  • Elias M, Wieczorek G, Rosenne S, Tawfik DS (2014) The universality of enzymatic rate–temperature dependency. Trends Biochem Sci 39:1–7

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Fonseca JS, Marangoni LFB, Marques JA, Bianchini A (2019a) Energy metabolism enzymes inhibition by the combined effects of increasing temperature and copper exposure in the coral Mussismilia harttii. Chemosphere 236:124420

    Article  Google Scholar 

  • García NAC, Campos JE, Musi JLT, Forsman ZH, Muñoz JLM, Reyes AM, González JEA (2017) Comparative molecular and morphological variation analysis of Siderastrea (Anthozoa, Scleractinia) reveals the presence of Siderastrea stellata in the Gulf of Mexico. Biol Bull 232:58–70

    Article  PubMed  Google Scholar 

  • Gattuso JP, Yellowlees D, Lesser M (1993) Scleractinian coral Stylophora pistillata. Mar Ecol Prog Ser 92:267–276

    Article  Google Scholar 

  • Goodbody-Gringley G, Waletich J (2018) Morphological plasticity of the depth generalist coral, Montastraea cavernosa, on mesophotic reefs in Bermuda. Ecology 99:1688–1690

    Article  PubMed  Google Scholar 

  • Grafen A (1989) The phylogenetic regression. Philos Trans R Soc Lond B Biol Sci 326:119–157

    Article  CAS  PubMed  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  CAS  PubMed  Google Scholar 

  • Hathaway JA, Atkinson DE (1965) Kinetics of regulatory enzymes: effect of adenosine triphosphate on yeast citrate synthase. Biochem Biophys Res Commun 20:661–665

    Article  CAS  PubMed  Google Scholar 

  • Hawkins TD, Hagemeyer JC, Hoadley KD, Marsh AG, Warner ME (2016) Partitioning of respiration in an animal-algal symbiosis: implications for different aerobic capacity between Symbiodinium spp. Front Physiol 7:128

    Article  PubMed  PubMed Central  Google Scholar 

  • Hennige SJ, Smith DJ, Perkins R, Consalvey M, Paterson DM, Suggett DJ (2008) Photoacclimation, growth and distribution of massive coral species in clear and turbid waters. Mar Ecol Prog Ser 369:77–88

    Article  Google Scholar 

  • Henry L (2013) Metabolism in corals from Antarctica, the deep-sea, and the shallow subtropics: contrasts in temperature, depth, and light. Ph.D. thesis, University of South Florida, p 86

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford, p 479

    Google Scholar 

  • Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    Article  PubMed  Google Scholar 

  • Hughes AD, Grottoli AG (2013b) Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS ONE 8:e81172

    Article  PubMed  PubMed Central  Google Scholar 

  • Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

    Article  CAS  PubMed  Google Scholar 

  • IPCC 2014 Climate Change (2014) Synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Painel on Climate Change [Core Writing]

  • Kitahara MV, Fukami H, Benzoni F, Huang D (2016) The new systematics of Scleractinia: integrating molecular and morphological evidence. In: The Cnidaria, past, present and futureSpringer, Cham

  • Klymasz-Swartz AK, Allen GJ, Treberg JR, Yoon GR, Tripp A, Quijada-Rodriguez AR, Weihrauch D (2019) Impact of climate change on the American lobster (Homarus americanus): physiological responses to combined exposure of elevated temperature and pCO2. Comp Biochem Physiol Mol Integr Physiol 235:202–210

    Article  CAS  Google Scholar 

  • Lallier FH, Walsh PJ (1991) Metabolic potential in tissues of the blue crab, Callinectes sapidus. Bull Mar Sci 48:665–669

    Google Scholar 

  • Lauer MM, de Oliveira CB, Yano NLI, Bianchini A (2012) Copper effects on key metabolic enzymes and mitochondrial membrane potential in gills of the estuarine crab Neohelice granulata at different salinities. Comp Biochem Physiol C Toxicol Pharmacol 156:140–147

    Article  CAS  PubMed  Google Scholar 

  • Leão ZM, Kikuchi RK, Oliveira MD (2019) Chapter 35 The coral reef province of Brazil. World Seas: an environmental evaluation. Elsevier, New York, pp 813–833

    Chapter  Google Scholar 

  • Leão ZM, Kikuchi RK and Testa V (2003) Corals and coral reefs of Brazil. In: Latin American coral reefs. Elsevier Science, pp 9–52

  • Leão ZM, Kikuchi RKP, Oliveira MD, Vasconcellos V (2010) Status of Eastern Brazilian coral reefs in time of climate changes. Pan-Am J Aquat Sci 5:224–235

    Google Scholar 

  • Leão ZM, Kikuchi RK, Ferreira BP, Neves EG, Sovierzoski HH, Oliveira MD, Maida M, Correia MD, Johnsson R (2016) Brazilian coral reefs in a period of global change: a synthesis. Braz J Oceanogr 64:97–116

    Article  Google Scholar 

  • Lewis JB (2006) Biology and ecology of the hydrocoral Millepora on coral reefs. Adv Mar Biol 50:1–55

    Article  PubMed  Google Scholar 

  • Lindenfors P, Revell LJ, Nunn CL (2010) Sexual dimorphism in primate aerobic capacity: a phylogenetic test. J Evol Biol 23:1183–1194

    Article  PubMed  PubMed Central  Google Scholar 

  • Linsmayer LB, Deheyn DD, Tomanek L, Tresguerres M (2020) Dynamic regulation of coral energy metabolism throughout the diel cycle. Sci Rep 10:19881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131

    Article  Google Scholar 

  • Marangoni LFB, Mies M, Güth AZ, Banha TN, Inague A, Fonseca JDS, Bianchini A (2019) Peroxynitrite generation and increased heterotrophic capacity are linked to the disruption of the coral–dinoflagellate symbiosis in a scleractinian and hydrocoral species. Microorganisms 7:426

    Article  PubMed Central  Google Scholar 

  • Mies M, Francini-Filho RB, Zilberberg C, Garrido AG, Longo GO, Laurentino E, Banha TN (2020) South Atlantic coral reefs are major global warming refugia and less susceptible to bleaching. Front Mar Sci 7:514

    Article  Google Scholar 

  • Mies M, Güth AZ, Tenório AA, Banha TNS, Waters LG, Polito PS, Sumida PYG (2018) In situ shifts of predominance between autotrophic and heterotrophic feeding in the reef-building coral Mussismilia hispida: an approach using fatty acid trophic markers. Coral Reefs 37:677–689

    Article  Google Scholar 

  • Morley SA, Lurman GJ, Skepper JN, Pörtner HO, Peck LS (2009) Thermal plasticity of mitochondria: a latitudinal comparison between Southern Ocean molluscs. Comp Biochem Physiol A Mol Integr Physiol 152:423–430

    Article  PubMed  Google Scholar 

  • Nelson DL, Cox MM (2021) Lehninger: principles of biochemistry, 8th edn. Freeman, New York, p 1248

    Google Scholar 

  • Pace DA, Marsh AG, Leong PK, Green AJ, Hedgecock D, Manahan DT (2006) Physiological bases of genetically determined variation in growth of marine invertebrate larvae: a study of growth heterosis in the bivalve Crassostrea gigas. J Exp Mar Biol Ecol 335:188–209

    Article  Google Scholar 

  • Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamian corals. Mar Ecol Prog Ser 300:79–89

    Article  Google Scholar 

  • Paradis E, Schliep K (2018) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: linear and nonlinear mixed effects models_. R package version 3.1-96 URL: https://CRAN.R-project.org/package=nlme

  • Pörtner H (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Article  PubMed  Google Scholar 

  • Pörtner H, Bock C, Mark FC (2017) Oxygen-and capacity-limited thermal tolerance: bridging ecology and physiology. J Exp Biol 220:2685–2696

    Article  PubMed  Google Scholar 

  • Putnam HM, Barott KL, Ainsworth TD, Gates RD (2017) The vulnerability and resilience of reef-building corals. Curr Biol 27:R528–R540

    Article  CAS  PubMed  Google Scholar 

  • Revell LJ (2010) Phylogenetic signal and linear regression on species data. Methods Ecol Evol 1:319–329

    Article  Google Scholar 

  • Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Rezende EL, Diniz-Filho JAF (2012) Phylogenetic analyses: comparing species to infer adaptations and physiological mechanisms. Compr Physiol 2:639–674

    Article  PubMed  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882

    Article  Google Scholar 

  • Schoepf V, Grottoli AG, Warner ME, Cai WJ, Melman TF, Hoadley KD, Wang Y (2013c) Correction: Coral energy reserves and calcification in a high-CO 2 world at two temperatures. PLoS ONE 9:e108082

    Google Scholar 

  • Segel IH (1975) Enzyme kinetics: behavior and analysis of rapid equilibrium and steady state enzyme systems. N Y 115:A472–A473

    Google Scholar 

  • Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15

    Article  CAS  PubMed  Google Scholar 

  • Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53:597–608

    Article  PubMed  Google Scholar 

  • Souza JN, Nunes FL, Zilberberg C, Sanchez JA, Migotto AE, Hoeksema BW, Lindner A (2017) Contrasting patterns of connectivity among endemic and widespread fire coral species (Millepora spp.) in the tropical Southwestern Atlantic. Coral Reefs 36:701–716

    Article  Google Scholar 

  • Srere PA (1971) An eclectic view of metabolic regulation: control of citrate synthase activity. Adv Enzyme Regul 9:221–233

    Article  Google Scholar 

  • Storey KB, Brooks SP (1995) The basis of enzymatic adaptation. Princ Med Biol 44:147–169

    Article  Google Scholar 

  • Tedesco EC, Segal B, Calderon EN, Schiavetti A (2017) Conservation of Brazilian coral reefs in the Southwest Atlantic Ocean: a change of approach. Lat Am J Aquat Res 45:228–245

    Article  Google Scholar 

  • Teschima MM, Garrido A, Paris A, Nunes FL, Zilberberg C (2019b) Correction: Biogeography of the endosymbiotic dinoflagellates (Symbiodiniaceae) community associated with the brooding coral Favia gravida in the Atlantic Ocean. PLoS ONE 14:e0215167

    Article  PubMed  PubMed Central  Google Scholar 

  • Vasconcelos MJ, Leão ZM, Kikuchi RK (2018) Coral reef growth pattern in eastern Brazil has not changed since the Holocene. Quat Environ Geosci 9:49–61

    Google Scholar 

  • Vetter RAH (1995) Ecophysiological studies on citrate-synthase:(I) enzyme regulation of selected crustaceans with regard to temperature adaptation. J Comp Physiol B 165:46–55

    Article  CAS  Google Scholar 

  • Wiegand G, Remington SJ (1986) Citrate synthase: structure, control, and mechanism. Annu Rev Biophys Biophys Chem 15:97–117

    Article  CAS  PubMed  Google Scholar 

  • Weitzman PDJ, Danson MJ (1976) Citrate synthase. Curr Top Cell Regul 10:161–204

    Article  CAS  PubMed  Google Scholar 

  • Winter APM, Chaloub RM, Duarte GAS (2016) Photosynthetic responses of corals Mussismilia harttii (Verrill, 1867) from turbid waters to changes in temperature and presence/absence of light. Braz J Oceanogr 64:203–216

    Article  Google Scholar 

  • Woodhead AJ, Hicks CC, Norström AV, Williams GJ, Graham NA (2019) Coral reef ecosystem services in the Anthropocene. Funct Ecol 33:1023–1034

    Google Scholar 

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Acknowledgements

The present study was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Programa Ciências do Mar, Brasília, DF, Brazil; grant #1984/ 2014 to AB), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, #307647/2016-1 to AB), and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, #2017/05310-9 to SCF). We are grateful to Coral Vivo Project and its sponsors Petrobras (Programa Petrobras Ambiental) and Arraial d'Ajuda Eco Park. AB is a research fellow from CNPq (Proc. # 307647/2016-1). Corals were collected under MMA/ICMBio # 59974-1 and Secretaria Municipal de Porto Seguro #03/2017 permissions to SCF. We are indebted to C. Pereira, L. Santos and L. Marangoni for helping with field work, laboratory experiment and sample processing. This work constitutes part of a MSc dissertation submitted by MSA to the Graduate Program in Biological Oceanography, Instituto de Oceanografia, Universidade Federal do Rio Grande-FURG, Rio Grande, RS, Brazil.

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Angonese, M.S., Faria, S.C. & Bianchini, A. Is citrate synthase an energy biomarker in Southwestern Atlantic corals? A comparative, biochemical approach under a simulated scenario of climate change. Coral Reefs 41, 213–222 (2022). https://doi.org/10.1007/s00338-021-02215-6

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