Abstract
Scleractinian corals provide the three-dimensional structure and function of coral reefs around the globe. These sessile animals are subject to physical injuries from a variety of sources and can completely regenerate damaged tissue as a survival mechanism; however, tissue regeneration rates vary widely within and across taxa. To explore the intraspecific differences in tissue regeneration, circular lesions (12 mm diameter × 3 mm deep) were created on 30 Montastraea cavernosa colonies at a depth of 10–12 m in the coastal waters of Carriacou, Grenada. Coral regeneration was documented at weekly intervals for 33 d. Nonlinear regression was used to generate a predictive model for lesion closure with time, and separate models were fit to corals that regenerated normally and those that had significantly delayed regeneration. A lesion created on each coral colony was re-sampled at each of 14, 21, and 31, 32, or 33 d following injury, and the polyps were flash-frozen and stored for proteomic analysis. An initial polyp sample, the 14 d, the 21 d, and the 31–33 d samples were used to quantify the difference in protein abundance as the lesions healed using tandem mass tags and liquid chromatography-mass spectrometry. One hundred thirty-one proteins were significantly differentially abundant in ‘fast’ vs. ‘slow’ M. cavernosa colonies. These proteins have been associated with inflammation, the extracellular matrix, skeleton, catabolism, and apoptosis in other corals. Differences in the abundance of proteins in these categories may have led to the observed differences between regeneration in the ‘fast’ and ‘slow’ M. cavernosa colonies.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Aurora AB, Olson EN (2015) Immune modulation of stem cells and regeneration. Cell Stem Cell 15:14–25
Barneah O, Benayahu Y, Weis VM (2006) Comparative proteomics of symbiotic and aposymbiotic juvenile soft corals. Mar Biotechnol 8:11–16
Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: Does host genotype limit phenotypic plasticity? Mol Ecol 19:1705–1720
Baumgarten S, Simakov O, Esherick LY, Liew YJ, Lehnert EM, Michell CT, Li Y, Hambleton EA, Guse A, Oates ME, Gough J, Weis VM, Aranda M, Pringle JR, Voolstra CR (2015) The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc Natl Acad Sci 112:11893–11898
Bely AE, Nyberg KG (2010) Evolution of animal regeneration: re-emergence of a field. Trends Ecol Evol 25:161–170
Bommer UA, Thiele BJ (2004) The translationally controlled tumour protein (TCTP). Int J Biochem Cell Biol 36:379–385
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Casey TM, Khan JM, Bringans SD, Koudelka T, Takle PS, Downs RA, Livk A, Syme RA, Tan KC, Lipscombe RJ (2017) Analysis of reproducibility of proteome coverage and quantitation using isobaric mass tags (iTRAQ and TMT). J Proteome Res 16:384–392
Chang J, Musser JH, McGregor H (1987) Phospholipase A2: Function and pharmacological regulation. Biochem Pharmacol 36:2429–2436
Chiou CY, Chen IP, Chen C, Wu HJL, Wei NV, Wallace CC, Chen CA (2008) Analysis of Acropora muricata calmodulin (CaM) indicates that scleractinian corals possess the ancestral exon/intron organization of the eumetazoan CaM gene. J Mol Evol 66:317–324
Closek CJ, Sunagawa S, DeSalvo MK, Piceno YM, DeSantis TZ, Brodie EL, Weber MX, Voolstra CR, Andersen GL, Medina M (2014) Coral transcriptome and bacterial community profiles reveal distinct Yellow Band Disease states in Orbicella faveolata. ISME J 8:2411–2422
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676
Cox AD, Der CJ (2003) The dark side of Ras: Regulation of apoptosis. Oncogene 22:8999–9006
Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and pretome-wide protein quantification. Nat Biotechnol 26:1367–1372
Császár NBM, Seneca FO, Van Oppen MJH (2009) Variation in antioxidant gene expression in the scleractinian coral Acropora millepora under laboratory thermal stress. Mar Ecol Prog Ser 392:93–102
Cziesielski MJ, Liew YJ, Cui G, Schmidt-Roach S, Campana S, Marondedze C, Aranda M (2018) Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc R Soc B Biol Sci 285:20172654
DeBoer ML, Krupp DA, Weis VM (2007) Proteomic and transcriptional analyses of coral larvae newly engaged in symbiosis with dinoflagellates. Comp Biochem Physiol - Part D Genomics Proteomics 2:63–73
Drake J, Mass T, Haramaty L, Zelzion E, Bjattacharya D, Falkowski P (2013) Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata. Proc Natl Acad Sci 110:3788–3793
Fuess LE, Pinzón JH, Weil E, Mydlarz LD (2016) Associations between transcriptional changes and protein phenotypes provide insights into immune regulation in corals. Dev Comp Immunol 62:17–28
Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435
Hayward DC, Hetherington S, Behm CA, Grasso LC, Forêt S, Miller DJ, Ball EE (2011) Differential gene expression at coral settlement and metamorphosis - a subtractive hybridization study. PLoS One 6:e26411
Henry LA, Hart M (2005) Regeneration from injury and resource allocation in sponges and corals - A review. Int Rev Hydrobiol 90:125–158
Horricks RA, Herbinger CM, Lillie BN, Taylor P, Lumsden JS (2019) Differential protein abundance during the first month of regeneration of the Caribbean star coral Montastraea cavernosa. Coral Reefs 38:45–61
Huang C, Morlighem JÉRL, Cai J, Liao Q, Perez CD, Gomes PB, Guo M, Rádis-Baptista G, Lee SMY (2017) Identification of long non-coding RNAs in two anthozoan species and their possible implications for coral bleaching. Sci Rep 7:1–18
Joshi R, Gilligan DM, Otto E, McLaughlin T, Bennett V (1991) Primary structure and domain organization of human alpha and beta adducin. J Cell Biol 115:665–675
Kitchen SA, Crowder CM, Poole AZ, Weis VM, Meyer E (2015) De novo assembly and characterization of four Anthozoan (phylum Cnidaria) transcriptomes. G3 Bethesda 5:2441–2452
Koch C, Anderson D, Moran M, Ellis C, Pawson T (2006) SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252:668–674
De La Cruz EM, Ostap EM, Brundage RA, Reddy KS, Sweeney HL, Safer D (2000) Thymosin-β4 changes the conformation and dynamics of actin monomers. Biophys J 78:2516–2527
Lee JH, Rho SB, Chun T (2005) Programmed cell death 6 (PDCD6) protein interacts with death-associated protein kinase 1 (DAPk1): Additive effect on apoptosis via caspase-3 dependent pathway. Biotechnol Lett 27:1011–1015
Lesser MP, Shick JM (1989) Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity. Mar Biol 102:243–255
Li W, Ye Y (2008) Polyubiquitin chains: Functions, structures, and mechanisms. Cell Mol Life Sci 65:2397–2406
Low TL, Liu DT, Jou JH (1992) Primary structure of thymosin β 12, a new member of the β-thymosin family isolated from perch liver. Arch Biochem Biophys 293:32–39
Lupi A, Tenni R, Rossi A, Cetta G, Forlino A (2008) Human prolidase and prolidase deficiency: An overview on the characterization of the enzyme involved in proline recycling and on the effects of its mutations. Amino Acids 35:739–752
Mass T, Drake JL, Haramaty L, Rosenthal Y, Schofield OME, Sherrell RM, Falkowski PG (2012) Aragonite precipitation by “proto-polyps” in coral cell cultures. PLoS One 7:8–15
Mayfield AB, Hsiao YY, Fan TY, Chen CS, Gates RD (2010) Evaluating the temporal stability of stress-activated protein kinase and cytoskeleton gene expression in the Pacific reef corals Pocillopora damicornis and Seriatopora hystrix. J Exp Mar Bio Ecol 395:215–222
Mydlarz LD, Palmer CV (2011) The presence of multiple phenoloxidases in Caribbean reef-building corals. Comp Biochem Physiol - Part A 159:372–378
Nevalainen TJ, Peuravuori HJ, Quinn RJ, Llewellyn LE, Benzie JAH, Fenner PJ, Winkel KD (2004) Phospholipase A2 in Cnidaria. Comp Biochem Physiol - B Biochem Mol Biol 139:731–735
Otto JJ (1990) Vinculin. Cell Motil Cytoskeleton 16:1–6
Palmer CV, Modi CK, Mydlarz LD (2009) Coral fluorescent proteins as antioxidants. PLoS One 4:e7298
Peng SE, Chen WNU, Chen HK, Lu CY, Mayfield AB, Fang LS, Chen CS (2011) Lipid bodies in coral-dinoflagellate endosymbiosis: Proteomic and ultrastructural studies. Proteomics 11:3540–3555
Peng SE, Luo YJ, Huang HJ, Lee IT, Hou LS, Chen WNU, Fang LS, Chen CS (2008) Isolation of tissue layers in hermatypic corals by N-acetylcysteine: Morphological and proteomic examinations. Coral Reefs 27:133–142
Peng SE, Wang YB, Wang LH, Chen WNU, Lu CY, Fang LS, Chen CS (2010) Proteomic analysis of symbiosome membranes in cnidaria - Dinoflagellate endosymbiosis. Proteomics 10:1002–1016
Pollack K, Balazs K, Ogunseitan O (2009) Proteomic assessment of caffeine effects on coral symbionts. Environ Sci Technol 43:2085–2091
Rahman MA, Isa Y (2005) Characterization of proteins from the matrix of spicules from the alcyonarian, Lobophytum crassum. J Exp Mar Bio Ecol 321:71–82
Rahman MA, Oomori T (2009) Analysis of protein-induced calcium carbonate crystals in soft coral by near-field IR microspectroscopy. Anal Sci 25:153–155
Reef R, Dunn S, Levy O, Dove S, Shemesh E, Brickner I, Leggat W, Hoegh-Guldberg O (2009) Photoreactivation is the main repair pathway for UV-induced DNA damage in coral planulae. J Exp Biol 212:2760–2766
Richardson CA, Dustan P, Lang JC (1979) Maintenance of living space by sweeper tentacles of Montastrea cavenosa, a Caribbean Reef Coral. Mar Biol 186:181–186
Romanova EV, Roth MJ, Rubakhim SS, Jakuboski JA, Kelley WP, Kirk MD, Kelleher NL, Sweedler JV (2006) Identification and characterization of homologues of vertebrate β-thymosin in the marine mollusk Aplysia californica. J Mass Spectrom 41:1030–1040
Rougée LRA, Richmond RH, Collier AC (2014) Natural variations in xenobiotic-metabolizing enzymes: Developing tools for coral monitoring. Coral Reefs 33:523–535
Slattery M, Ankisetty S, Corrales J, Marsh-Hunkin KE, Gochfeld DJ, Willett KL, Rimoldi JM (2012) Marine proteomics: A critical assessment of an emerging technology. J Nat Prod 75:1833–1837
Stoeva S, Horger S, Voelter W (1997) A novel β-thymosin from the sea urchin: Extending the phylogenetic distribution of β-thymosins from mammals to echinoderms. J Pept Sci 3:282–290
Sun Y, Chen X, Xu Y, Liu Q, Jiang X, Wang S, Guo W, Zhou Y (2017) Thymosin β4 is involved in the antimicrobial immune response of Golden pompano, Trachinotus ovatus. Fish Shellfish Immunol 69:90–98
Sunagawa S, DeSalvo MK, Voolstra CR, Reyes-Bermudez A, Medina M (2009) Identification and gene expression analysis of a taxonomically restricted cysteine-rich protein family in reef-building corals. PLoS One 4:e4865
Surazynski A, Donald SP, Cooper SK, Whiteside MA, Salnikow K, Liu Y, Phang JM (2008) Extracellular matrix and HIF-1 signaling: The role of prolidase. Int J Cancer 122:1435–1440
Swulius MT, Waxham MN (2008) Ca2 +/calmodulin-dependent protein kinases. Cell Mol Life Sci 65:2637–2657
Technau U, Steele RE (2011) Evolutionary crossroads in developmental biology: Cnidaria. Development 138:1447–1458
Van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883
Vigneswara V, Lowenson JD, Powell CD, Thakur M, Bailey K, Clarke S, Ray DE, Carter WG (2006) Proteomic identification of novel substrates of a protein isoaspartyl methyltransferase repair enzyme. J Biol Chem 281:32619–32629
Voolstra CR, Sunagawa S, Matz MV, Bayer T, Aranda M, Buschiazzo E, DeSalvo MK, Lindquist E, Szmant AM, Coffroth MA, Medina M (2011) Rapid evolution of coral proteins responsible for interaction with the environment. PLoS One 6:e20392
van De Water JAJAM, Ainsworth TD, Leggat W, Bourne DG, Willis BL, Van Oppen MJH (2015a) The coral immune response facilitates protection against microbes during tissue regeneration. Mol Ecol 24:3390–3404
van de Water JAJAM, Leggat W, Bourne DG, van Oppen MJH, Willis BL, Ainsworth TD (2015b) Elevated seawater temperatures have a limited impact on the coral immune response following physical damage. Hydrobiologia 759:201–214
Wenger Y, Buzgariu W, Reiter S, Galliot B (2014) Injury-induced immune responses in Hydra. Semin Immunol 26:277–294
Weston AJ, Dunlap WC, Beltran VH, Starcevic A, Hranueli D, Ward M, Long PF (2015) Proteomics Links the Redox State to Calcium Signaling During Bleaching of the Scleractinian Coral Acropora microphthalma on Exposure to High Solar Irradiance and Thermal Stress. Mol Cell Proteomics 14:585–595
Weston AJ, Dunlap WC, Shick JM, Klueter A, Iglic K, Vukelic A, Starcevic A, Ward M, Wells ML, Trick CG, Long PF (2012) A profile of an endosymbiont-enriched fraction of the coral Stylophora pistillata reveals proteins relevant to microbial-host interactions. Mol Cell Proteomics 11:M111.015487
Wilkinson DM (1999) The disturbing history of intermediate disturbance. Oikos 84:145–147
Wojdyla K, Rogowska-Wrzesinska A, Wrzesinski K, Roepstorff P (2011) Mass spectrometry based approach for identification and characterisation of fluorescent proteins from marine organisms. J Proteomics 75:44–55
Woo S, Lee A, Denis V, Chen CA, Yum S (2014) Transcript response of soft coral (Scleronephthya gracillimum) on exposure to polycyclic aromatic hydrocarbons. Environ Sci Pollut Res 21:901–910
Yan L, Fei K, Bridge D, Sarras MP (2000) A cnidarian homologue of translationally controlled tumor protein (P23/TCTP). Dev Genes Evol 210:507–511
Zacharias H, Anokhin B, Khalturin K, Bosch TCG (2004) Genome sizes and chromosomes in the basal metazoan Hydra. Zoology 107:219–227
Zhang J, Xin L, Shan B, Chen W, Xie M, Yuen D, Zhang W, Zhang Z, Lajoie GA, Ma B (2012) PEAKS DB: De novo sequencing assisted database search for sensitive and accurate peptide identification. Mol Cell Proteomics 11(M111):010587
Zhang X, Guo L, Collage RD, Stripay JL, Tsung A, Lee JS, Rosengart MR (2011) Calcium/calmodulin-dependent protein kinase (CaMK) I mediates the macrophage inflammatory response to sepsis. J Leukoc Biol 90:249–261
Acknowledgements
We would like to thank Annette Patrick and Deefer Diving Carriacou for their help with the collection of samples in the field and Bioinformatics Solutions Inc. and Dyanne Brewer for their technical assistance interpreting LC–MS data. Funding for this research was provided by a NSERC Discovery Grant (Lumsden) and St. George’s University. Horricks received an OVC Scholarship and is the recipient of a St. George’s University post-doctoral scholarship.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Topic Editor Simon Davy
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Horricks, R.A., Herbinger, C.M., Vickaryous, M.K. et al. Differential protein abundance associated with delayed regeneration of the scleractinian coral Montastraea cavernosa. Coral Reefs 39, 1175–1186 (2020). https://doi.org/10.1007/s00338-020-01952-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-020-01952-4