Abstract
In corals, different biological processes are associated with the daily variation of temperature and light, which in shallow reefs can vary widely and regularly reach extreme levels. The expression of cellular defense mechanisms such as the heat shock proteins Hsp70 and Hsp60 was analyzed in coral colonies adapted to live in a shallow lagoon, during three consecutive days characterized by the same temperature/light trend. Each of the three species investigated showed a significant diel modulation of both Hsps, which also displayed a coordinated expression. However, the diel modulations of both Hsps were species specific and only that of the branching Acropora tenuis appeared correlated with the temperature. All the species displayed high Hsp levels at 13.00 and 16.00, probably as protection for the cellular stress produced by the elevated temperature and light. Taken together, the results may provide useful information about the cellular mechanisms involved in the corals adaptation to extreme conditions.
Similar content being viewed by others
References
Balchin D, Hayer-Hartl M, Hartl FU (2016) In vivo aspects of protein folding and quality control. Science 353:4354
Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA 110:1387–1392
Bhagooli R, Hidaka M (2004) Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stresses. Comp Biochem Physiol A 137:547–555
Brady AK, Snyder KA, Vize PD (2011) Circadian cycles of gene expression in the coral, Acropora millepora. PLoS One. https://doi.org/10.1371/journal.pone.0025072
Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99–105
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
Camp EF, Nitschke MR, Rodolfo-Metalpa R, Houlbreque F, Gardner SG, Smith DJ, Zampighi M, Suggett DJ (2017) Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci Rep 7:2434
Camp EF, Schoepf V, Mumby PJ, Hardtke LA, Rodolfo-Metalpa R, Smith DJ, Suggett DJ (2018) The future of coral reefs subject to rapid climate change: lessons from natural extreme environments. Front Mar Sci 5:4
Chow AM, Ferrier-Pagès C, Khalouei S, Reynaud S, Brown IR (2009) Increased light intensity induces heat shock protein Hsp60 in coral species. Cell Stress Chaperones 14:469–476
Craig P, Birkeland C, Belliveau S (2001) High temperatures tolerated by a diverse assemblage of shallow-water corals in American Samoa. Coral Reefs 20:185–189
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
Downs CA, Ostrander GK, Rougée LRA, Rongo T, Knutson S, Williams DE, Mendiola W, Holbrook J, Richmond RH (2012) The use of cellular diagnostics for identifying sublethal stress in reef corals. Ecotoxicology 21:768–782
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
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
Hemond EM, Vollmer SV (2015) Diurnal and nocturnal transcriptomic variation in the Caribbean staghorn coral, Acropora cervicornis. Mol Ecol 24:4460–4473
Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Progr Ser 183:73–86
Kalmar B, Greensmith L (2009) Induction of heat shock proteins for protection against oxidative stress. Adv Drug Deliv Rev 61:310–318
Kenkel CD, Matz MV (2016) Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat Ecol Evol 1:0014
Kenkel CD, Moya A, Strahl J, Humphrey C, Bay LK (2017) Functional genomic analysis of corals from natural CO2-seeps reveals core molecular responses involved in acclimatization to ocean acidification. Global Change Biol 24:158–171
Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278
Levy O, Achituv Y, Yacobi YZ, Dubinsky Z, Stambler N (2006) Diel tuning of coral metabolism: physiological responses to light cues. J Exp Biol 209:273–283
Levy O, Kaniewska P, Alon S et al (2011) Complex diel cycles of gene expression in coral-algal symbiosis. Science 331:175
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
McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Change 2:623
Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:444–456
Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898
Papp E, Nardai G, Soti C, Csermely P (2003) Molecular chaperones, stress proteins and redox homeostasis. Biofactors 17:249–257
Poli D, Fabbri E, Goffredo S, Airi V, Franzellitti S (2017) Physiological plasticity related to zonation affects hsp70 expression in the reef-building coral Pocillopora verrucosa. PloS One. https://doi.org/10.1371/journal.pone.0171456
Schneider K, Levy O, Dubinsky Z, Erez J (2009) In-situ diel cycles of photosynthesis and calcification in hermatypic corals. Limnol Oceanogr 54:1995–2002
Schoepf V, Stat M, Falter JL, McCulloch MT (2015) Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment. Sci Rep 5:17639
Seveso D, Montano S, Strona G, Orlandi I, Galli P, Vai M (2013) Exploring the effect of salinity changes on the levels of Hsp60 in the tropical coral Seriatopora caliendrum. Mar Environ Res 90:96–103
Seveso D, Montano S, Strona G, Orlandi I, Galli P, Vai M (2014) The susceptibility of corals to thermal stress by analyzing Hsp60 expression. Mar Environ Res 99:69–75
Seveso D, Montano S, Reggente MAL, Orlandi I, Galli P, Vai M (2015) The modulation of the Hsp60 in response to the coral Brown Band disease. Dis Aquat Org 115:15–23
Seveso D, Montano S, Reggente MAL, Maggioni D, Orlandi I, Galli P, Vai M (2017) The cellular stress response of the scleractinian coral Goniopora columna during the progression of the black band disease. Cell Stress Chaperones 22:225–236
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
Swain TD, Bold EC, Osborn PC, Baird AH, Westneat MW, Backman V, Marcelino LA (2018) Physiological integration of coral colonies is correlated with bleaching resistance. Mar Ecol Progr Ser 586:1–10
Thimijan RW, Heins RD (1983) Photometric, radiometric, and quantum light units of measure: a review of procedures for interconversion. HortScience 18:818–822
Vai M, Popolo L, Alberghina L (1986) Immunological cross-reactivity of fungal and yeast plasma membrane H+-ATPase. FEBS Lett 206:135–141
Yakovleva I, Hidaka M (2004) Diel fluctuations of mycosporine-like amino acids in shallow-water scleractinian corals. Mar Biol 145:863–873
Zhou M, Wu X, Ginsberg HN (1996) Evidence that a rapidly turning over protein, normally degraded by proteasomes, regulates hsp72 gene transcription in HepG2 cells. J Biol Chem 271:24769–24775
Acknowledgements
The authors wish to thank all the MaRHE Center staff for the logistical support provided and Neil Campbell for English editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Topic Editor Simon Davy
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Seveso, D., Montano, S., Maggioni, D. et al. Diel modulation of Hsp70 and Hsp60 in corals living in a shallow reef. Coral Reefs 37, 801–806 (2018). https://doi.org/10.1007/s00338-018-1703-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-018-1703-0