Abstract
It is critical to determine the methods by which coral colonies regenerate tissue lost to physical injury as they provide the physical structure of coral reef systems. To explore regeneration, circular lesions (12 mm diameter × 3 mm depth) were created in the fall of 2014 on 124 Montastraea cavernosa colonies located in the coastal waters of Grenada and Carriacou (10–12 m depth). Coral regeneration was documented at weekly intervals for 28 days. Repeated measures ANOVA on estimated weekly coral regeneration rates showed that island (p = 0.024) and colony colour (p = 0.024) were the only factors significantly affecting lesion regeneration. Mean rate of lesion closure during the first 28 days was approximately 2.8 mm2 d−1. Four identical circular lesions were created on 30 M. cavernosa colonies (Carriacou, 10–12 m depth) in the fall of 2015. One representative lesion created on each coral colony was re-sampled at each of 14, 21, and 32 or 33 days following injury, and coral tissue was flash-frozen. Tissues from 10 normally pigmented brown colonies were selected for proteomic analysis using tandem mass tags. The initial polyp sample, the day 14, and the final samples were used to quantify the difference in protein abundance as the lesions healed. In the tissue samples 6419 peptides were reliably identified, which corresponded to 906 unique proteins. During the first month of regeneration, 111 proteins were differentially abundant (p < 0.05) on at least one timepoint and of these, 11 were associated with regeneration. An additional 14 proteins were also identified that were differentially abundant (p < 0.05) and were associated with inflammation or antioxidant activity. This work demonstrates, for the first time, the differential abundance of proteins associated with regeneration in a scleractinian coral.
Similar content being viewed by others
References
Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with imageJ. Biophotonics Int 11:36–41
Alberts B (ed) (2002) Molecular biology of the cell, 4th edn. Garland Science, New York, NY
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Anderson R, Morrall C, Nimrod S, Balza R, Berg C, Jossart J (2012) Benthic and fish population monitoring associated with a marine protected area in the nearshore waters of Grenada, Eastern Caribbean. Int J Trop Biol 60:71–87
Anderson R, Morrall C, Nimrod S, Balza R, Berg C, Jossart J (2014) Marine Protected Area monitoring in the nearshore waters of Grenada, Eastern Caribbean: benthic cover and fish populations. Rev Biol Trop 62:71–87
Andrews SC (2010) The Ferritin-like superfamily: Evolution of the biological iron storeman from a rubrerythrin-like ancestor. Biochim Biophys Acta 1800:691–705
Aurora AB, Olson EN (2015) Immune modulation of stem cells and regeneration. Cell Stem Cell 15:14–25
Bak RPM, Meesters EH (1998) Coral population structure: The hidden information of colony size-frequency distributions. Mar Ecol Prog Ser 162:301–306
Bak RPM, Steward-Van Es Y (1980) Regeneration of superficial damage in the Scleractinian corals Agaricia agaricites F. Purpurea and Porites astreoides. Bull Mar Sci 30:883–887
Bak RPM, Brouns JJWM, Heys FML (1977) Regeneration and aspects of spatial competition in the scleractinian corals Agaricia agaricites and Montastrea annularis. In: Proceedings of 3rd international coral reef Symposium Miami, pp 143–148
Baldauf SL, Palmer JD, Doolittle WF (1996) The root of the universal tree and the origin of eukaryotes based on elongation factor phylogeny. Proc Natl Acad Sci USA 93:7749–7754
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
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
Brown BE, Bythell JC (2005) Perspectives on mucus secretion in reef corals. Mar Ecol Prog Ser 296:291–309
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
Bryer SC, Fantuzzi G, Van Rooijen N, Koh TJ (2008) Urokinase-type plasminogen activator plays essential roles in macrophage chemotaxis and skeletal muscle regeneration. J Immunol 180:1179–1188
Burton PM, Finnerty JR (2009) Conserved and novel gene expression between regeneration and asexual fission in Nematostella vectensis. Dev Genes Evol 219:79–87
Chang BY, Chiang M, Cartwright CA (2001) The interaction of Src and RACK1 is enhanced by activation of protein kinase C and tyrosine phosphorylation of RACK1. J Biol Chem 276:20346–20356
Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Arch Biochem Biophys 401:145–154
Chen B, Zhong D, Monteiro A (2006) Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BMC Genomics 7:156
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
Chow AM, Beraud E, Tang DWF, Ferrier-Pagès C, Brown IR (2012) Hsp60 protein pattern in coral is altered by environmental changes in light and temperature. Comp Biochem Physiol 161:349–353
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 J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and protome-wide protein quantification. Nat Biotechnol 26:1367–1372
Croquer A, Villamizar E, Noriega N (2002) Environmental factors affecting tissue regeneration of the reef-building coral Montastraea annularis (Faviidae) at Los Roques National Park, Venezuela. Revi Biol Trop 3:1055–1065
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
D’Angelo C, Smith EG, Oswald F, Burt J, Tchernov D, Wiedenmann J (2012) Locally accelerated growth is part of the innate immune response and repair mechanisms in reef-building corals as detected by green fluorescent protein (GFP)-like pigments. Coral Reefs 31:1045–1056
Dalton TP, Shertzer HG, Puga A (1999) Regulation of gene expression by reactive oxygen. Annu Rev Pharmacol Toxicol 39:67–101
Deininger MH, Meyermann R, Schluesener HJ (2002) The allograft inflammatory factor-1 family of proteins. FEBS Lett 514:115–121
Di Natale A (2017) Apolipoprotein domain containing proteins and innate immunity in rainbow trout and walleye. MSc thesis, University of Guelph
Downs CA, Mueller E, Phillips S, Fauth JE, Woodley CM (2000) A molecular biomarker system for assessing the health of coral (Montastraea faveolata) during heat stress. Mar Biotechnol 2:533–544
Downs CA, Fauth JE, Robinson CE, Curry R, Lanzendorf B, Halas JC, Halas J, Woodley CM (2005) Cellular diagnostics and coral health: Declining coral health in the Florida Keys. 51:558–569
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
Fisher EM, Fauth JE, Hallock P, Woodley CM (2007) Lesion regeneration rates in reef-building corals Montastraea spp. as indicators of colony condition. Mar Ecol Prog Ser 339:61–71
Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching. J Exp Mar Bio Ecol 373:102–110
Foster NL, Baums IB, Mumby PJ (2007) Sexual vs. asexual reproduction in an ecosystem engineer: The massive coral Montastraea annularis. J Anim Ecol 76:384–391
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
Galloway SB, Work TM, Bochsler VS, Harley RA, Kramarsky-Winters E, McLaughlin SM, Meteyer CU, Morado JF, Nicholson JH, Parnell PG, Peters EC, Reynolds TL, Rotstein DS, Sileo L, and Woodley CM (2007) Coral disease and health workshop: Coral histopathology II. NOAA Technical Memorandum NOS NCCOS 56 and NOAA Technical Memorandum CRCP 4. National Oceanic and Atmospheric Administration, Silver Spring, MD. 84p
Goffredo S, Vergni P, Reggi M, Caroselli E, Sparla F, Levy O, Goffredo S, Vergni P, Reggi M, Caroselli E, Sparla F, Levy O, Falini G (2011) The skeletal organic matrix from Mediterranean coral Balanophyllia europaea influences calcium carbonate precipitation. PLoS One 6:e22338
Goldberg WM (1974) Evidence of a sclerotized collagen from the skeleton of a gorgonian coral. Comp Biochem Physiol - Part B Biochem 49:525–526
Goss RJ (1992) The evolution of regeneration: Adaptive or inherent? J Theor Biol 159:241–260
Graham JE, van Woesik R (2013) The effects of partial mortality on the fecundity of three common Caribbean corals. Mar Biol 160:2561–2565
Hall VR (1997) Interspecific differences in the regeneration of artificial injuries on scleractinian corals. J Exp Mar Bio Ecol 212:9–23
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
Helman Y, Natale F, Sherrell RM, LaVigne M, Starovoytov V, Gorbunov MY, Falkowski PG (2008) Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro. Proc Natl Acad Sci 105:54–58
Henry LA, Hart M (2005) Regeneration from injury and resource allocation in sponges and corals - A review. Int Rev Hydrobiol 90:125–158
Jatkar A (2008) Mucus layer properties and dynamics in reef corals. Ph.D thesis, Newcastle University
Jatkar AA, Brown BE, Bythell JC, Guppy R, Morris NJ (2010) Coral Mucus: The properties of its constituent mucins. Biomacromolecules 11:883–888
Kitchen SA, Crowder CM, Poole AZ, Weis VM, Meyer E (2015) De novo assembly and characterization of four Anthozoan (phylum Cnidaria) transcriptomes. G3 5:2441–2452
Kramarsky-Winter E, Loya Y (2000) Tissue regeneration in the coral Fungia granulosa: The effect of extrinsic and intrinsic factors. Mar Biol 137:867–873
Lesser MP (2004) Experimental biology of coral reef ecosystems. J Exp Mar Bio Ecol 300:217–252
Lesser MP (2006) Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu Rev Physiol 68:253–278
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
Marshall PA (2000) Skeletal damage in reef corals: relating resistance to colony morphology. Mar Ecol Prog Ser 200:177–189
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
Mayfield AB, Wang LH, Tang PC, Fan TY, Hsiao YY, Tsai CL, Chen CS (2011) Assessing the impacts of experimentally elevated temperature on the biological composition and molecular chaperone gene expression of a reef coral. PLoS One 6:e26529
Meesters EH, Bak RP (1993) Effects of coral bleaching on tissue regeneration potential and colony survival. 96:189–198
Meesters EH, Noordeloos M, Bak RPM (1994) Damage and regeneration: Links to growth in the reef-building coral Montastrea annularis. Mar Ecol Prog Ser 112:119–128
Meesters EH, Wesseling I, Bak RPM (1996) Reef-building corals and the relation with colony morphology. Bull Mar Sci 58:838–852
Meesters EH, Pauchli W, Bak RPM (1997) Predicting regeneration of physical damage on a reef-building coral by regeneration capacity and lesion shape. Mar Ecol Prog Ser 146:91–99
Meikle P, Richards GN, Yellowlees D (1988) Structural investigations on the mucus from six species of coral. Mar Biol 99:187–193
Miller DJ, Ball EE, Forêt S, Satoh N (2011) Coral genomics and transcriptomics - Ushering in a new era in coral biology. J Exp Mar Bio Ecol 408:114–119
Mydlarz LD, Palmer CV (2011) The presence of multiple phenoloxidases in Caribbean reef-building corals. Comp Biochem Physiol – Part A 159:372–378
Nagelkerken I, Bak R (1998) Differential regeneration of artificial lesions among sympatric morphs of the Caribbean corals Porites astreoides and Stephanocoenia michelinii. Mar Ecol Prog Ser 171:279–283
Novak ML, Bryer SC, Cheng M, Nguyen M-H, Conley KL, Cunningham AK, Xue B, Sisson TH, You J-S, Hornberger TA, Koh TJ (2011) Macrophage-specific expression of urokinase-type plasminogen activator promotes skeletal muscle regeneration. J Immunol 187:1448–1457
Palmer CV, Modi CK, Mydlarz LD (2009) Coral fluorescent proteins as antioxidants. PLoS One 4:e7298
Palmer CV, Traylor-Knowles NG, Willis BL, Bythell JC (2011) Corals use similar immune cells and wound-healing processes as those of higher organisms. PLoS One 6:e23992
PEAKS Team (2013) PEAKS 7 User Manual. Waterloo, ON
Polato NR, Voolstra CR, Schnetzer J, DeSalvo MK, Randall CJ, Szmant AM, Medina M, Baums IB (2010) Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS One 5:e11221
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Renegar D-EA (2015) Histology and ultrastructure of Montastraea cavernosa and Porites astreoides during regeneration and recruitment: Anthropogenic stressors and transplant success. Ph.D. thesis, Nova State University
Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14
Robbart ML, Peckol P, Scordilis SP, Curran HA, Brown-Saracino J (2004) Population recovery and differential heat shock protein expression for the corals Agaricia agaricites and A. tenuifolia in Belize. Mar Ecol Prog Ser 283:151–160
Rodríguez-Martínez RE, Jordan-Garza AG, Jordan-Dahlgren E (2016) Low regeneration of lesions produced by coring in Orbicella faveolata. Peer J 4:e1596
Rodríguez-Villalobos JC, Work TM, Calderon-Aguilera LE (2016) Wound repair in Pocillopora. J Invertebr Pathol 139:1–5
Rossi S, Snyder MJ (2001) Competition for space among sessile marine invertebrates: changes in HSP70 expression in two pacific Cnidarians. Biol Bull 201:385–393
Roth MS, Latz MI, Goericke R, Deheyn DD (2010) Green fluorescent protein regulation in the coral Acropora yongei during photoacclimation. J Exp Biol 213:3644–3655
Rougée LRA, Richmond RH, Collier AC (2014) Natural variations in xenobiotic-metabolizing enzymes: Developing tools for coral monitoring. Coral Reefs 33:523–535
Sabine AM, Smith TB, Williams DE, Brandt ME (2015) Environmental conditions influence tissue regeneration rates in scleractinian corals. Mar Poll Bull 95:253–264
Sabourault C, Ganot P, Deleury E, Allemand D, Furla P (2009) Comprehensive EST analysis of the symbiotic sea anemone, Anemonia viridis. BMC Genomics 10:333
Seveso D, Montano S, Strona G, Orlandi I, Vai M, Galli P (2012) Up-regulation of Hsp60 in response to skeleton eroding band disease but not by algal overgrowth in the scleractinian coral Acropora muricata. Mar Environ Res 78:34–39
Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: A possible first line of defense. FEMS Microbiol Ecol 67:371–380
Siboni N, Abrego D, Motti CA, Tebben J, Harder T (2014) Gene expression patterns during the early stages of chemically induced larval metamorphosis and settlement of the coral Acropora millepora. PLoS One 9:e91082
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
Soderhall K, Smith VJ (eds) (1986) Hemocytic and humoral immunity in arthropods. Wiley, New York, pp 251–286
Squires DF (1958) Stony corals from the vicinity of Bimini, Bahamas, British West Indies. Bull Am Museum Nat Hist 115:215–262
Stenken JA, Poschenrieder AJ (2015) Bioanalytical chemistry of cytokines-a review. Anal Chim Acta 853:95–115
Stevens FC (1982) Calmodulin: an introduction. Can J Biochem Cell Biol 61:906–910
Sunagawa S, DeSalvo MK, Voolstra CR, Reyes-Bermudez A, Medina M (2009a) Identification and gene expression analysis of a taxonomically restricted cysteine-rich protein family in reef-building corals. PLoS One 4:e4865
Sunagawa S, Wilson EC, Thaler M, Smith ML, Caruso C, Pringle JR, Weis VM, Medina M, Schwarz JA (2009b) 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
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
Teitelbaum SL (2000) Bone resorption by osteoclasts. Science 289:1504–1508
Thompson A, Schäfer JJ, Kuhn K, Kienle S, Schwarz J, Schmidt GG, Neumann T, Hamon C (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75:1895–1904
Turk V, Stoka V, Vasiljeva O, Renko M, Sun T, Turk B, Turk D (2012) Cysteine cathepsins: From structure, function and regulation to new frontiers. Biochim Biophys Acta - Proteins Proteomics 1824:68–88
Van Veghel MLJ, Bak RPM (1994) Reproductive characteristics of the polymorphic Caribbean reef building coral Montastrea annularis III. Fecundity and colony structure. Mar Ecol Ser 109:221–227
Van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883
van De Water JAJM, 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 JAJM, 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
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
Watanabe Y, Tateno H, Nakamura-Tsuruta S, Kominami J, Hirabayashi J, Nakamura O, Watanabe T, Kamiya H, Naganuma T, Ogawa T, Naudé RJ, Muramoto K (2009) The function of rhamnose-binding lectin in innate immunity by restricted binding to Gb3. Dev Comp Immunol 33:187–197
Wenger Y, Buzgariu W, Reiter S, Galliot B (2014) Injury-induced immune responses in Hydra. Semin Immunol 26:277–294
Whitten MMA, Tew IF, Lee BL, Ratcliffe NA (2004) A novel role for an insect apolipoprotein (Apolipophorin III) in β-1,3-glucan pattern recognition and cellular encapsulation reactions. J Immunol 172:2177–2185
Wickham H (2016) Elegant graphics for data analysis. Springer-Verlag, New York
Wootton EC, Pipe RK (2003) Structural and functional characterisation of the blood cells of the bivalve mollusc, Scrobicularia plana. Fish Shellfish Immunol 15:249–262
Work TM, Aeby GS (2010) Wound repair in Montipora capitata. J Invert Pathol 105:116–119
Young JAC (1974) The nature of tissue regeneration after wounding in the sea anemone Callactis parasitica (Couch). J Mar Biol Assoc UK 54:599–617
Zhang X, Guo L, Collage RD, Stripay JL, Tsung A, Lee JS, Rosengart MR (2011) Calcium/calmodulin-dependent protein kinase (CaMK) Iα mediates the macrophage inflammatory response to sepsis. J Leukoc Biol 90:249–261
Zhou Z, Yu X, Tang J, Zhu Y, Chen G, Guo L, Huang B (2017) Dual recognition activity of a rhamnose-binding lectin to pathogenic bacteria and zooxanthellae in stony coral Pocillopora damicornis. Dev Comp Immunol 70:88–93
Acknowledgements
We would like to thank Annette Patrick, Deefer Diving Carriacou, and EcoDive Grenada for their help with the collection of samples in the field, 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.
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 Morgan S. Pratchett
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Horricks, R.A., Herbinger, C.M., Lillie, B.N. et al. Differential protein abundance during the first month of regeneration of the Caribbean star coral Montastraea cavernosa. Coral Reefs 38, 45–61 (2019). https://doi.org/10.1007/s00338-018-01754-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-018-01754-9