Abstract
The green filamentous endolithic alga Ostreobium quekettii 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 Porites lutea and Goniastrea perisi 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.
References
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 72:3016–3020
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 275:89–95
Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order : Scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254–260
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 273:2305–2312
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326
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 Oceanography
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 392:1–15
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 280:456–468
Famà P, Wysor B, Kooistra W, Zuccarello GC (2002) Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplat tufA gene. J Phycol 38:1040–1050
Fine M, Loya Y (2002) Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc Lond B Biol Sci 269:1205–1210
Fine M, Steindler L, Loya Y (2004) Endolithic algae photoacclimate to increased irradiance during coral bleaching. Mar Freshw Res 55:115–121
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 208:75–81
Fine M, Roff G, Ainsworth TD, Hoegh-Guldberg O (2006) Phototrophic microendoliths bloom during coral “white syndrome”. Coral Reefs 25:577–581
Forsterra F, Haussermann V (2008) Unusual symbiotic relationships between microendolithic phototrophic organisms and azooxanthellate cold-water corals from Chilean fjords. Mar Ecol Prog Ser 370:121–125
Fricke HW, Knauer B (1986) Diversity and spatial pattern of coral communities in the Red-Sea Upper Twilight Zone. Oecologia 71:29–37
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 53:43–55
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp 41:95–98
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 10:968–978
Highsmith RC (1981) Lime-boring algae in coral skeletons. J Exp Mar Biol Ecol 55:267–281
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
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 301:929–933
Johannes RE, Wiebe WJ (1970) A method for determination of coral tissue biomass and composition. Limnol Oceanogr 15:822–824
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
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 317:67–73
LaJeunesse TC, Trench RK (2000) Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biol Bull 199:126–134
Lam DW, Zechman FW (2006) Phylogenetic analyses of the Bryopsidales (Ulvophyceae, Chlorophyta) based on RUBISCO large subunit gene sequences. J Phycol 42:669–678
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 117:137–147
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 117:149–157
Littman RA, Willis BL, Bourne DG (2009) Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389:45–59
Lukas KJ (1974) Two species of the chlorophyte genus Ostreobium from skeletons of Atlantic and Caribbean reef corals. J Phycol 10:331–335
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)
Pochon X, LaJeunesse TC, Pawlowski J (2004) Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar Biol 146:17–27
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 136:19–27
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 152:395–404
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 265–278
Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91
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 5:355–362
Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc Natl Acad Sci USA 92:2850–2853
Schlichter D, Zscharnack B, Krisch H (1995) Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82:561–564
Schlichter D, Kampmann H, Conrady S (1997) Trophic potential and photoecology of endolithic algae living within coral skeletons. Mar Ecol 18:299–317
Swofford DL (1998) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) v4.0.b10. Sinauer, Sunderland
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596
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 155:353–361
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 24:422–434
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 21:424–432
Tribollet A, Langdon C, Golubic S, Atkinson M (2006) Endolithic microflora major primary producers in dead carbonate substrates of Hawaiian coral reefs. J Phycol 42:292–303
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: GB3008
Ulstrup KE, Kuhl M, Bourne DG (2007) Zooxanthellae harvested by ciliates associated with brown band syndrome of corals remain photosynthetically competent. Appl Environ Microb 73:1968
Van Oppen MJH (2004) Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Mar Biol 144:1–7
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 41:126–139
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 44:240–254
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 45:726–731
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 50:642–653
Weil E, Smith G, Gil-Agudelo DL (2006) Status and progress in coral reef disease research. Dis Aquat Org 69:1–7
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 384:107–119
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 51:99–123
Woolcott GW, Knoller K, King RJ (2000) Phylogeny of the Bryopsidaceae (Bryopsidales, Chlorophyta): cladistic analyses of morphological and molecular data. Phycologia 39:471–481
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 73:2755
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Gutner-Hoch, E., Fine, M. Genotypic diversity and distribution of Ostreobium quekettii within scleractinian corals. Coral Reefs 30, 643–650 (2011). https://doi.org/10.1007/s00338-011-0750-6
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DOI: https://doi.org/10.1007/s00338-011-0750-6