Coral Reefs

, Volume 30, Issue 3, pp 643–650 | Cite as

Genotypic diversity and distribution of Ostreobium quekettii within scleractinian corals

Report

Abstract

The green filamentous endolithic alga Ostreobiumquekettii resides inside skeletons of scleractinian corals in close proximity with their tissue and plays a role in the viability of the coral and its associates. This study examined the distribution and diversity of O.quekettii within scleractinian corals from the Red Sea (Eilat, Gulf of Aqaba), using a molecular phylogenetic marker. The massive coral species Poriteslutea and Goniastreaperisi were sampled from a depth range of 6–55 m, and ribulose 1,5-bisphosphate carboxylase large subunit gene (rbcL) DNA sequence of the alga was amplified and analyzed for diversity and distribution of ecological patterns. This work reveals that O. quekettii has at least seven different clades distributed along a depth gradient in the examined scleractinian corals. Among the seven identified clades, four were found only in P. lutea, while the other two clades are found in both P. lutea and G. perisi. Goniastrea perisi colonies at depth of 30 m had a distinct O. quekettii clade that was absent in P. lutea. It is obvious from this study that the green endolithic alga O.quekettii is not a single genotype as previously considered but a complex of genotypes and that this differentiation is of ecological significance.

Keywords

Holobiont Endolithic alga Scleractinian coral Ribulose 1 5-bisphosphate carboxylase large subunit gene (rbcLClade 

References

  1. Ainsworth TD, Fine M, Blackall LL, Hoegh-Guldberg O (2006) Fluorescence in situ hybridization and spectral imaging of coral-associated bacterial communities. Appl Environ Microbiol 72:3016–3020CrossRefPubMedPubMedCentralGoogle Scholar
  2. Barneah O, Weis VM, Perez S, Benayahu Y (2004) Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Mar Ecol Prog Ser 275:89–95CrossRefGoogle Scholar
  3. Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order : Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254–260CrossRefPubMedGoogle Scholar
  4. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc B 273:2305–2312CrossRefPubMedPubMedCentralGoogle Scholar
  5. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326CrossRefGoogle Scholar
  6. Carilli JE (2009) Century-scale records of coral growth and water quality from the Mesoamerican reef reveal increasing anthropogenic stress and decreasing coral resilience. Ph.D. dissertation, UC San Diego: Scripps Institution of OceanographyGoogle Scholar
  7. Carreiro-Silva M, McClanahan TR, Kiene WE (2009) Effects of inorganic nutrients and organic matter on microbial euendolithic community composition and microbioerosion rates. Mar Ecol Prog Ser 392:1–15CrossRefGoogle Scholar
  8. Chazottes V, Cabioch G, Golubic S, Radtke G (2009) Bathymetric zonation of modern microborers in dead coral substrates from New Caledonia–Implications for paleodepth reconstructions in Holocene corals. Palaeogeogr Palaeocl 280:456–468CrossRefGoogle Scholar
  9. Famà P, Wysor B, Kooistra W, Zuccarello GC (2002) Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplat tufA gene. J Phycol 38:1040–1050CrossRefGoogle Scholar
  10. Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc Lond B Biol Sci 269:1205–1210CrossRefGoogle Scholar
  11. Fine M, Steindler L, Loya Y (2004) Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar Freshw Res 55:115–121CrossRefGoogle Scholar
  12. Fine M, Meroz-Fine E, Hoegh-Guldberg O (2005) Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. J Exp Biol 208:75–81CrossRefPubMedGoogle Scholar
  13. Fine M, Roff G, Ainsworth TD, Hoegh-Guldberg O (2006) Phototrophic microendoliths bloom during coral “white syndrome”. Coral Reefs 25:577–581CrossRefGoogle Scholar
  14. Forsterra F, Haussermann V (2008) Unusual symbiotic relationships between microendolithic phototrophic organisms and azooxanthellate cold-water corals from Chilean fjords. Mar Ecol Prog Ser 370:121–125CrossRefGoogle Scholar
  15. Fricke HW, Knauer B (1986) Diversity and spatial pattern of coral communities in the Red-Sea Upper Twilight Zone. Oecologia 71:29–37CrossRefPubMedGoogle Scholar
  16. Gektidis M, Dubinsky Z, Goffredo S (2007) Microendoliths of the Shallow Euphotic Zone in open and shaded habitats at 30 degrees N - Eilat, Israel - paleoecological implications. Facies 53:43–55CrossRefGoogle Scholar
  17. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp 41:95–98Google Scholar
  18. Händeler KHA, Wägele HWA, Wahrmund UTE, Rüdinger MRU, Knoop V (2010) Slugs’ last meals: molecular identification of sequestered chloroplasts from different algal origins in Sacoglossa (Opisthobranchia, Gastropoda). Mol Ecol Resour 10:968–978CrossRefPubMedGoogle Scholar
  19. Highsmith RC (1981) Lime-boring algae in coral skeletons. J Exp Mar Biol Ecol 55:267–281CrossRefGoogle Scholar
  20. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  21. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedGoogle Scholar
  22. Johannes RE, Wiebe WJ (1970) A method for determination of coral tissue biomass and composition. Limnol Oceanogr 15:822–824CrossRefGoogle Scholar
  23. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  24. Kramarsky-Winter E, Harel M, Siboni N, Ben Dov E, Brickner I, Loya Y, Kushmaro A (2006) Identification of a protist-coral association and its possible ecological role. Mar Ecol Prog Ser 317:67–73CrossRefGoogle Scholar
  25. LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134CrossRefPubMedGoogle Scholar
  26. Lam DW, Zechman FW (2006) Phylogenetic analyses of the Bryopsidales (Ulvophyceae, Chlorophyta) based on RUBISCO large subunit gene sequences. J Phycol 42:669–678CrossRefGoogle Scholar
  27. Le Campion-Alsumard T, Golubic S, Priess K (1995a) Fungi in corals - Symbiosis or disease - Interaction between polyps and fungi causes pearl-like skeleton biomineralization. Mar Ecol Prog Ser 117:137–147CrossRefGoogle Scholar
  28. Le Campion-Alsumard T, Golubic S, Hutchings P (1995b) Microbial endoliths in skeletons of live and dead corals - Porites lobata (Moorea, French-Polynesia). Mar Ecol Prog Ser 117:149–157CrossRefGoogle Scholar
  29. Littman RA, Willis BL, Bourne DG (2009) Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389:45–59CrossRefGoogle Scholar
  30. Lukas KJ (1974) Two species of the chlorophyte genus Ostreobium from skeletons of Atlantic and Caribbean reef corals. J Phycol 10:331–335Google Scholar
  31. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in coral reefs. In: Dubinsky Z (ed) Coral reefs. Elsevier, Amsterdam (Ecosystems of the World, vol 25, pp 75–87)Google Scholar
  32. Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27CrossRefGoogle Scholar
  33. Priess K, Le Campion-Alsumard T, Golubic S, Gadel F, Thomassin BA (2000) Fungi in corals: black bands and density-banding of Porites lutea and P. lobata skeleton. Mar Biol 136:19–27CrossRefGoogle Scholar
  34. Ralph PJ, Larkum AWD, Kuhl M (2007) Photobiology of endolithic microorganisms in living coral skeletons: 1. Pigmentation, spectral reflectance and variable chlorophyll fluorescence analysis of endoliths in the massive corals Cyphastrea serailia, Porites lutea and Goniastrea australensis. Mar Biol 152:395–404CrossRefGoogle Scholar
  35. Rohwer F, Kelley S (2004) Culture-independent analyses of coral-associated microbes. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer, Heidelberg, pp 265–278CrossRefGoogle Scholar
  36. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91CrossRefGoogle Scholar
  37. Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362CrossRefPubMedGoogle Scholar
  38. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853CrossRefPubMedPubMedCentralGoogle Scholar
  39. Schlichter D, Zscharnack B, Krisch H (1995) Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82:561–564CrossRefGoogle Scholar
  40. Schlichter D, Kampmann H, Conrady S (1997) Trophic potential and photoecology of endolithic algae living within coral skeletons. Mar Ecol 18:299–317CrossRefGoogle Scholar
  41. Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) v4.0.b10. Sinauer, SunderlandGoogle Scholar
  42. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596Google Scholar
  43. Titlyanov EA, Kiyashko SI, Titlyanova TV, Kalita TL, Raven JA (2008) 13 C and 15 N values in reef corals Porites lutea and P. cylindrica and in their epilithic and endolithic algae. Mar Biol 155:353–361CrossRefGoogle Scholar
  44. Tribollet A, Golubic S (2005) Cross-shelf differences in the pattern and pace of bioerosion of experimental carbonate substrates exposed for 3 years on the northern Great Barrier Reef, Australia. Coral Reefs 24:422–434CrossRefGoogle Scholar
  45. Tribollet A, Decherf G, Hutchings PA, Peyrot-Clausade M (2002) Large-scale spatial variability in bioerosion of experimental coral substrates on the Great Barrier Reef (Australia): importance of microborers. Coral Reefs 21:424–432Google Scholar
  46. Tribollet A, Langdon C, Golubic S, Atkinson M (2006) Endolithic microflora major primary producers in dead carbonate substrates of Hawaiian coral reefs. J Phycol 42:292–303CrossRefGoogle Scholar
  47. Tribollet A, Godinot C, Atkinson MJ, Langdon C (2009) Effects of elevated pCO2 on dissolution of coral carbonates by microbial euendoliths. Global Biogeochem Cycles 23: GB3008Google Scholar
  48. Ulstrup KE, Kuhl M, Bourne DG (2007) Zooxanthellae harvested by ciliates associated with brown band syndrome of corals remain photosynthetically competent. Appl Environ Microb 73:1968CrossRefGoogle Scholar
  49. Van Oppen MJH (2004) Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Mar Biol 144:1–7CrossRefGoogle Scholar
  50. Verbruggen H, De Clerck O, Cocquyt E, Kooistra W, Coppejans E (2005) Morphometric taxonomy of siphonous green algae: A methodological study within the genus Halimeda (Bryopsidales). J Phycol 41:126–139CrossRefGoogle Scholar
  51. Verbruggen H, Leliaert F, Maggs CA, Shimada S, Schils T, Provan J, Booth D, Murphy S, De Clerck O, Littler DS, Littler MM, Coppejans E (2007) Species boundaries and phylogenetic relationships within the green algal genus Codium (Bryopsidales) based on plastid DNA sequences. Mol Phylogenet Evol 44:240–254CrossRefPubMedGoogle Scholar
  52. Verbruggen H, Vlaeminck C, Sauvage T, Sherwood AR, Leliaert F, De Clerck O (2009a) Phylogenetic analysis of Pseudochlorodesmis strains reveals cryptic diversity above the family level in the siphonous green algae (Bryopsidales, Chlorophyta). J Phycol 45:726–731CrossRefPubMedGoogle Scholar
  53. Verbruggen H, Ashworth M, LoDuca ST, Vlaeminck C, Cocquyt E, Sauvage T, Zechman FW, Littler DS, Littler MM, Leliaert F (2009b) A multi-locus time-calibrated phylogeny of the siphonous green algae. Mol Phylogenet Evol 50:642–653CrossRefPubMedGoogle Scholar
  54. Weil E, Smith G, Gil-Agudelo DL (2006) Status and progress in coral reef disease research. Dis Aquat Org 69:1–7CrossRefPubMedGoogle Scholar
  55. Winters G, Beer S, Zvi BB, Brickner I, Loya Y (2009) Spatial and temporal photoacclimation of Stylophora pistillata: zooxanthella size, pigmentation, location and clade. Mar Ecol Prog Ser 384:107–119CrossRefGoogle Scholar
  56. Wisshak M, Gektidis M, Freiwald A, Lundalv T (2005) Bioerosion along a bathymetric gradient in a cold-temperate setting (Kosterfjord, SW Sweden): an experimental study. Facies 51:99–123CrossRefGoogle Scholar
  57. Woolcott GW, Knoller K, King RJ (2000) Phylogeny of the Bryopsidaceae (Bryopsidales, Chlorophyta): cladistic analyses of morphological and molecular data. Phycologia 39:471–481CrossRefGoogle Scholar
  58. Yarden O, Ainsworth TD, Roff G, Leggat W, Fine M, Hoegh-Guldberg O (2007) Increased prevalence of ubiquitous Ascomycetes in an acropoid coral (Acropora formosa) exhibiting symptoms of brown band syndrome and skeletal eroding band disease. Appl Environ Microb 73:2755CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.The Mina & Everard Goodman Faculty of Life ScienceBar-Ilan UniversityRamat-GanIsrael
  2. 2.The Interuniversity Institute for Marine ScienceEilatIsrael

Personalised recommendations