Coral Reefs

, Volume 25, Issue 4, pp 531–543

Comprehensive characterization of skeletal tissue growth anomalies of the finger coral Porites compressa

  • Isabelle J. Domart-Coulon
  • Nikki Traylor-Knowles
  • Esther Peters
  • David Elbert
  • Craig A. Downs
  • Kathy Price
  • Joanne Stubbs
  • Shawn McLaughlin
  • Evelyn Cox
  • Greta Aeby
  • P. Randy Brown
  • Gary K. Ostrander
Report

Abstract

The scleractinian finger coral Porites compressa has been documented to develop raised growth anomalies of unknown origin, commonly referred to as “tumors”. These skeletal tissue anomalies (STAs) are circumscribed nodule-like areas of enlarged skeleton and tissue with fewer polyps and zooxanthellae than adjacent tissue. A field survey of the STA prevalence in Oahu, Kaneohe Bay, Hawaii, was complemented by laboratory analysis to reveal biochemical, histological and skeletal differences between anomalous and reference tissue. MutY, Hsp90a1, GRP75 and metallothionein, proteins known to be up-regulated in hyperplastic tissues, were over expressed in the STAs compared to adjacent normal-appearing and reference tissues. Histological analysis was further accompanied by elemental and micro-structural analyses of skeleton. Anomalous skeleton was of similar aragonite composition to adjacent skeleton but more porous as evidenced by an increased rate of vertical extension without thickening. Polyp structure was retained throughout the lesion, but abnormal polyps were hypertrophied, with increased mass of aboral tissue lining the skeleton, and thickened areas of skeletogenic calicoblastic epithelium along the basal floor. The latter were highly metabolically active and infiltrated with chromophore cells. These observations qualify the STAs as hyperplasia and are the first report in poritid corals of chromophore infiltration processes in active calicoblastic epithelium areas.

Keywords

Hyperplasia Coral disease Skeletal tissue Chromophore cells Porites compressa 

References

  1. Alker AP, Kim K, Dube DH, Harvell DC (2004) Localized induction of a generalized response against multiple biotic agents in Caribbean sea fans. Coral Reefs 23:397–405CrossRefGoogle Scholar
  2. Bak RPM (1983) Neoplasia, regeneration and growth in the reef-building coral Acropora palmata. Mar Biol 77:221–227CrossRefGoogle Scholar
  3. Barnes DJ, Lough JM (1992) Systematic variations in the depth of skeleton occupied by coral tissue in massive colonies of Porites from the Great Barrier Reef. J Exp Mar Biol Ecol 159:113–128CrossRefGoogle Scholar
  4. Breitbart M, Bhagooli R, Griffin S, Johnston I, Rohwer F (2005) Microbial communities associated with skeletal tumors on Porites compressa. FEMS Microbiol Lett 243:431–436CrossRefGoogle Scholar
  5. Caplin AJ, Jackson S, Smith D (2003) Hsp90 reaches new heights. EMBO Rep 4:126–130CrossRefGoogle Scholar
  6. Chalker B, Barnes D, Isdale P (1985) Calibration of X-ray densitometry for the measurement of coral skeletal density. Coral Reefs 4:95–100CrossRefGoogle Scholar
  7. Cheney D (1975) Hard tissue tumors of scleractinian corals. In: Hildemann WH, Benedict AA (eds) Immunologic phylogeny. Plenum, New York pp 77–87Google Scholar
  8. Cherian MG, Jayasurya A, Bay BH (2003) Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat Res 533(1–2):201–209Google Scholar
  9. Cohen AL, Smith SR, McCartney MS, van Etten J (2004) How brain corals record climate: an integration of skeletal structure, growth, and chemistry of Diploria labyrinthiformis from Bermuda. Mar Ecol Prog Ser 271:147–158Google Scholar
  10. Coles SL, Seapy DG (1998) Ultra-violet absorbing compounds and tumorous growths on acroporid corals from Bandar Khayran, Gulf of Oman, Ocean Indian. Coral Reefs 17:195–198CrossRefGoogle Scholar
  11. Coyle P, Philcox JC, Carey LC, Rofe AM (2002) Metallothionein: the multipurpose protein. Cell Mol Life Sci 59:627–647CrossRefGoogle Scholar
  12. De Carlo EH, BeltranVL, Tomlinson MS (2004) Composition of water and suspended sediment in streams of urbanized subtropical watersheds in Hawaii. Appl Geochem 19:1011–1037CrossRefGoogle Scholar
  13. Domart-Coulon I, Sinclair C, Hill R, Tambutté S, Puverel S, Ostrander GK (2004) A basidiomycete isolated from the skeleton of Pocillopora damicornis (Scleractinia) selectively stimulates short-term survival of coral skeletogenic cells. Mar Biol 144:83–592CrossRefGoogle Scholar
  14. Downs CA (2005) Cellular diagnostics and its application to aquatic and marine toxicology. In: Ostrander GK (ed) Techniques in aquatic toxicology, vol 2. CRC, Boca Raton, pp 181–208Google Scholar
  15. Duerden JE (1903) West Indian Madreporian Polyps. In: Memoirs of the National Academy of Sciences, Vol. VIII. Washington Government Printing Office, p 439 and plate IVGoogle Scholar
  16. Gateno D, Israel A, Barki Y, Rinkevich B (1998) Gastrovascular circulation in an octocoral: evidence of significant transport of coral and symbiont cells. Biol Bull 194:178–186CrossRefGoogle Scholar
  17. Gateno D, Leon A, Barki Y, Rinkevich B (2003) Skeletal tumor formations in the massive coral Pavona clavus. Mar Ecol Prog Ser 258:97–108Google Scholar
  18. Ghosh S, Gepstein S, Heikkala JJ Dumbroff BG (1988) Use of a scanning densitometer or an ELISA plate reader for measurement of nanogram amounts of protein in crude extracts from biological tissue. Anal Biochem 169:227–233CrossRefGoogle Scholar
  19. Gladfelter EH (1983) Circulation of fluids in the gastrovascular system of the reef coral Acropora cervicornis. Biol Bull 165:619–636CrossRefGoogle Scholar
  20. Goldberg WM, Makemson JC, Colley SB (1984) Entocladia endozoica sp nov., a pathogenic Chlorophyte: structure, life history, physiology, and effects on its coral host. Biol Bull 166:368–383CrossRefGoogle Scholar
  21. Grottoli AG (1999) Variability of stable isotopes and maximum linear extension in reef–coral skeletons at Kaneohe Bay, Hawaii. Mar Biol 135:437–449CrossRefGoogle Scholar
  22. Grygier MJ, Cairns SD (1996) Suspected neoplasms in deep-sea corals (Scleractinia: Oculinidae: Madrepora spp.) reinterpreted as galls caused by Petrarca madreporae n. sp. (Crustacea: Ascothoracida: Petrarcidae). Dis Aquat Org 24:61–69Google Scholar
  23. Haq F, Mahoney M, Koropatnick J (2003) Signaling events for metallothionein induction. Mutat Res 533:211–226Google Scholar
  24. Holt SE, Aisner DL, Baur J, Tesmer VM, Dy M, Ouellette M, Trager J, Morin GB, Toft DO, Shay JW, Wright WE, White MA (1999) Functional requirement of p23 and Hsp90 in telomerase complexes. Genes Dev 13:817–826Google Scholar
  25. Hunter C, Field SN (1997) Characterization of tumors in Porites corals. Am Zool 37:55Google Scholar
  26. Kondoh M, Imada N, Kamada K, Tsukahara R, Higashimoto M, Takiguchi M, Watanabe Y, Sato M (2003) Property of metallothionein as a Zn pool differs depending on the induced condition of metallothionein. Toxicol Lett 30(142):11–18CrossRefGoogle Scholar
  27. Le Campion-Alsumard T, Golubic S, Priess K (1995) Fungi in corals: symbiosis or disease? Interaction between polyps and fungi causes pearl-like skeleton biomineralization. Mar Ecol Prog Ser 117:137–147Google Scholar
  28. Loya Y, Bull G, Pichon M. (1984) Tumor formations in scleractinian corals. Helgol Meeresunters 37:99–112CrossRefGoogle Scholar
  29. Maret W (2000) The function of zinc metallothionein: a link between cellular zinc and redox state. J Nutr 130:1455–1458Google Scholar
  30. Maret W (2003) Cellular zinc and redox states converge in the metallothionein/thionein pair. J Nutr 133:1460S–1462SGoogle Scholar
  31. Marsh J (1969) Primary productivity of reef-building calcareous red algae. Ecology 51:255–263CrossRefGoogle Scholar
  32. Marshall AT, Wright OP (1993) Confocal laser scanning light microscopy of the extra-thecal epithelia of undecalcified scleractinian corals. Cell Tissue Res 272:533–543CrossRefGoogle Scholar
  33. Merks RMH, Hoekstra AG, Kaandorp JA, Sloot PMA (2004) Polyp oriented modelling of coral growth. J Theor Biol 228:559–576CrossRefGoogle Scholar
  34. Meszaros A, Bigger C (1999) Qualitative and quantitative study of wound healing processes in the coelenterate Plexaurella fusifera: spatial temporal and environmental (light attenuation) influences. J Invertebr Pathol 73:321–331CrossRefGoogle Scholar
  35. Morse DE, Morse ANC, Duncan H (1977) Algal “tumors” in the Caribbean sea fan, Gorgonia ventalina. Proc 3rd Int Coral Reef Symp 1:623–629Google Scholar
  36. Mullen K, Peters E, Harvell D (2004) Coral resistance to disease. In: Rosenberg E, Loya Y (eds) Coral disease and health, Springer, Berlin Heidelberg New York, pp 377–399Google Scholar
  37. Nichols W, Shade P, Hunt C (1996) Summary of the O’ahu, Hawai’i, Regional Aquifer-System Analysis. U.S. Geological Survey Professional Paper 1412-AGoogle Scholar
  38. Oren U, Benayahu Y, Lubinevsky H, Loya Y (2001) Colony integration during regeneration in the stony coral Favia favus. Ecology 82:802–813Google Scholar
  39. Peters EC, Halas JC, McCarty HB (1986) Calicoblastic neoplasms in Acropora palmata, with a review of reports on anomalies of growth and form in corals. J Natl Cancer Inst 76:895–912Google Scholar
  40. Peters EC, Price KL, Borsay-Horowitz DJ (2005) Histological preparation of invertebrates for evaluating contaminant effects. In: Ostrander GK (ed) Techniques in aquatic toxicology, vol 2. CRC, Boca Raton, pp 653–686Google Scholar
  41. Petes LE, Harvell CD, Peters EC, Webb MAH, Mullen KM (2003) Pathogens compromise reproduction and induce melanization in Caribbean sea fans. Mar Ecol Prog Ser 264:167–171Google Scholar
  42. Regala RP, Rice CD (2004) Mycobacteria, but not mercury, induces metallothionein (MT) protein in striped bass, Morone saxitilis, phagocytes, while both stimuli induce MT in channel catfish, Ictalurus punctatus, phagocytes. Mar Environ Res 58:719–723CrossRefGoogle Scholar
  43. Ringuet S, Mackenzie FT (2005) Controls on nutrient and phytoplankton dynamics by storm runoff events, southern Kaneohe Bay, Hawaii. Estuaries In pressGoogle Scholar
  44. Ravindran J, Raghukumar C, Raghukumar S (2001) Fungi in Porites lutea: association with healthy and diseased corals. Dis Aquat Org 47:219–228Google Scholar
  45. Rohringer R, Kim WK, Samborski DJ, Howes NK (1977) Calcofluor-optical brightener for fluorescence microscopy of fungal plant parasites in leaves. Phytopathology 67:808–810CrossRefGoogle Scholar
  46. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396:336–342CrossRefGoogle Scholar
  47. Simpkins C, Balderman S, Mensah E (1998) Mitochondrial oxygen consumption is synergistically inhibited by metallothionein and calcium. J Surg Res 80:16–21CrossRefGoogle Scholar
  48. Smith GW, Harvell CD, Kim K, Ritchie KB, James SC, Buchan KC (1998) Cellular events occurring during the pathogenesis of aspergillosis of Gorgonia species. In: Proceedings of the 7th Symposium on the Natural History of the Bahamas. Rev Biol Trop 46:205–208Google Scholar
  49. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Co, New YorkGoogle Scholar
  50. Squires D (1965) Neoplasia in a Coral?. Science 148:503–505CrossRefGoogle Scholar
  51. Srokowski T, Pfeifer JD, Li J, Olson LM, Radar JS (2004). Expression and localization of GRP75 in human epithelial tumors and normal tissues. Appl Immunohistochem Mol Morphol 12:132–138Google Scholar
  52. Sutherland KP, Porter J W, Torres C (2004) Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Mar Ecol Prog Ser 266:273–302Google Scholar
  53. Wadhwa R, Taira K, Kaul SC (2002) An Hsp70 family chaperone, mortalin/mthsp70/PBP74/GRP75: what, when, and where? Cell Stress Chaperones 7:309–316Google Scholar
  54. White P (1965) Abnormal Corallites. Science 150:77–78CrossRefGoogle Scholar
  55. Wielgus J, Glassom D (2002) An aberrant growth form of red sea corals caused by polychaete infestations. Coral Reefs 21:315–316Google Scholar
  56. Wilson WH, Dale AL, Davy JE, Davy SK (2005) An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145–148CrossRefGoogle Scholar
  57. Work TM, Rameyer RA (2005) Characterizing lesions in corals from American Samoa. Coral Reefs 24:384–390CrossRefGoogle Scholar
  58. Yamashiro H, Yamamoto M, van Woesik R (2000) Tumor formation on the Coral Montipora informis. Dis Aquat Org 41:211–217Google Scholar
  59. Yamashiro H, Hirosuke O, Onaga K, Iwasaki H, Takara K (2001) Coral tumors store reduced levels of lipids. J Exp Mar Biol Ecol 265:171–179CrossRefGoogle Scholar
  60. Ye B, Maret W, Vallee BL (2001) Zinc metallothionein imported into liver mitochondria modulates respiration. Proc Natl Acad Sci USA 98:2317–2322CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Isabelle J. Domart-Coulon
    • 1
  • Nikki Traylor-Knowles
    • 2
  • Esther Peters
    • 3
    • 4
  • David Elbert
    • 5
  • Craig A. Downs
    • 6
  • Kathy Price
    • 7
  • Joanne Stubbs
    • 5
  • Shawn McLaughlin
    • 7
  • Evelyn Cox
    • 8
  • Greta Aeby
    • 8
  • P. Randy Brown
    • 10
  • Gary K. Ostrander
    • 2
    • 9
    • 10
    • 11
  1. 1.Département Milieux et Peuplements Aquatiques, UMR 5178 BOMEMuseum National d’Histoire NaturelleParisFrance
  2. 2.Department of BiologyJohns Hopkins UniversityMDUSA
  3. 3.Tetra Tech, Inc.FairfaxUSA
  4. 4.Registry of Tumors in Lower AnimalsSterlingUSA
  5. 5.Department of Earth and Planetary SciencesJohns Hopkins UniversityBaltimoreUSA
  6. 6.Haereticus Environmental LaboratoryCliffordUSA
  7. 7.NOAA NOS Cooperative Oxford LaboratoryOxfordUSA
  8. 8.Hawaii Institute of Marine BiologyKaneoheUSA
  9. 9.Pacific Biosciences Research CenterUniversity of Hawaii at ManoaHonoluluUSA
  10. 10.Department of Comparative MedicineJohns Hopkins UniversityBaltimoreUSA
  11. 11.HonoluluUSA

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