Discordant coral–symbiont structuring: factors shaping geographical variation of Symbiodinium communities in a facultative zooxanthellate coral genus, Oculina
Tóm tắt
Understanding the factors that help shape the association between corals and their algal symbionts, zooxanthellae (Symbiodinium), is necessary to better understand the functional diversity and acclimatization potential of the coral host. However, most studies focus on tropical zooxanthellate corals and their obligate algal symbionts, thus limiting our full comprehension of coral–algal symbiont associations. Here, we examine algal associations in a facultative zooxanthellate coral. We survey the Symbiodinium communities associated with Oculina corals in the western North Atlantic and the Mediterranean using one clade-level marker (psbA coding region) and three fine-scale markers (cp23S–rDNA, b7sym15 flanking region, and b2sym17). We ask whether Oculina spp. harbor geographically different Symbiodinium communities across their geographic range and, if so, whether the host’s genetics or habitat differences are correlated with this geographical variation. We found that Oculina corals harbor different Symbiodinium communities across their geographical range. Of the habitat differences (including chlorophyll a concentration and depth), sea surface temperature is better correlated with this geographical variation than the host’s genetics, a pattern most evident in the Mediterranean. Our results suggest that although facultative zooxanthellate corals may be less dependent on their algal partners compared to obligate zooxanthellate corals, the Symbiodinium communities that they harbor may nevertheless reflect acclimatization to environmental variation among habitats.
Tài liệu tham khảo
Armoza-Zvuloni R, Segal R, Kramarsky-Winter E, Loya Y (2011) Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: Oculina patagonica as a model. Mar Ecol Prog Ser 426:149–159
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Baird AH, Guest JR, Willis BL (2009) Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu Rev Ecol Syst 40:551–571
Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Coral reefs: corals’ adaptive response to climate change. Nature 430:741
Barbrook AC, Visram S, Douglas AE, Howe CJ (2006) Molecular diversity of dinoflagellate symbionts of Cnidaria: the psbA minicircle of Symbiodinium. Protist 157:159–171
Baums I, Johnson M, Devlin-Durante M, Miller M (2010) Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean. Coral Reefs 29:835–842
Baums IB, Devlin-Durante MK, LaJeunesse TC (2014) New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies. Mol Ecol 23:4203–4215
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300
Berkelmans R, Van Oppen MJ (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 Lond B: Biol Sci 273:2305–2312
Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS One 5:e10871
Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562
Brooke S, Young CM (2003) Reproductive ecology of a deep-water scleractinian coral, Oculina varicosa, from the southeast Florida shelf. Cont Shelf Res 23:847–858
Brooke S, Young C (2005) Embryogenesis and larval biology of the ahermatypic scleractinian Oculina varicosa. Mar Biol 146:665–675
Chen CA, Wang J-T, Fang L-S, Yang Y-W (2005) Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Mar Ecol Prog Ser 295:113–121
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Dimond J, Carrington E (2007) Temporal variation in the symbiosis and growth of the temperate scleractinian coral Astrangia poculata. Mar Ecol Prog Ser 348:161–172
Dimond J, Kerwin A, Rotjan R, Sharp K, Stewart F, Thornhill D (2013) A simple temperature-based model predicts the upper latitudinal limit of the temperate coral Astrangia poculata. Coral Reefs 32:401–409
Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson A (2010) Geneious version 4.5.5. http://www.geneious.com
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Mol Ecol 18:2375–2389
Fabricius K, Mieog J, Colin P, Idip D, Van Oppen M (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13:2445–2458
Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709
Fine M, Loya Y (1995) The coral Oculina patagonica: a new immigrant to the Mediterranean coast of Israel. Israel J Zool 41:81
Fine M, Zibrowius H, Loya Y (2001) Oculina patagonica: a non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar Biol 138:1195–1203
Finney JC, Pettay DT, Sampayo EM, Warner ME, Oxenford HA, LaJeunesse TC (2010) The relative significance of host–habitat, depth, and geography on the ecology, endemism, and speciation of coral endosymbionts in the genus Symbiodinium. Microb Ecol 60:250–263
Glynn PW (1984) Widespread coral mortality and the 1982–83 El Niño warming event. Environ Conserv 11:133–146
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162
Howells E, Beltran V, Larsen N, Bay L, Willis B, Van Oppen M (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120
Iglesias-Prieto R, Trench RK (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates II. Response of chlorophyll-protein complexes to different photon-flux densities. Mar Biol 130:23–33
Jones AM, Berkelmans R, van Oppen MJ, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond B: Biol Sci 275:1359–1365
Keshavmurthy S, Hsu CM, Kuo CY, Meng PJ, Wang JT, Chen CA (2012) Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas. Mol Ecol 21:4393–4407
Koren O, Rosenberg E (2006) Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl Environ Microbiol 72:5254–5259
LaJeunesse T (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400
LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880
LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol 48:1380–1391
LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt G, Fitt W, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161
Leydet KP, Hellberg ME (2015) The invasive coral Oculina patagonica has not been recently introduced to the Mediterranean from the western Atlantic. BMC Evol Biol 15:79
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190
McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460
Parkinson JE, Baums IB (2014) The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front Microbiol 5:445
Parkinson JE, Coffroth MA, LaJeunesse TC (2015) New species of Clade B Symbiodinium (Dinophyceae) from the greater Caribbean belong to different functional guilds: S. aenigmaticum sp. nov., S. antillogorgium sp. nov., S. endomadracis sp. nov., and S. pseudominutum sp. nov. J Phycol 51:850–858
Pettay DT, Lajeunesse TC (2007) Microsatellites from clade B Symbiodinium spp. specialized for Caribbean corals in the genus Madracis. Mol Ecol Notes 7:1271–1274
Pettay DT, Wham DC, Pinzon JH, Lajeunesse TC (2011) Genotypic diversity and spatial–temporal distribution of Symbiodinium clones in an abundant reef coral. Mol Ecol 20:5197–5212
Pinzon JH, LaJeunesse TC (2011) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Mol Ecol 20:311–325
Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497
Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ 2:e394
Prada C, McIlroy SE, Beltrán DM, Valint DJ, Ford SA, Hellberg ME, Coffroth MA (2014) Cryptic diversity hides host and habitat specialization in a gorgonian–algal symbiosis. Mol Ecol 23:3330–3340
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reed JK (1981) In situ growth rates of the scleractinian coral Oculina varicosa occurring with zooxanthellae on 6-m reefs and without on 80-m banks. Proc 4th Int Coral Reef Symp 2:201–206
Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow water corals and other cnidarians. Proc Nat Acad Sci USA 105:13674–13678
Rodolfo-Metalpa R, Reynaud S, Allemand D, Ferrier-Pagès C (2008) Temporal and depth responses of two temperate corals, Cladocora caespitosa and Oculina patagonica, from the North Mediterranean Sea. Mar Ecol Prog Ser 369:103–114
Rodolfo-Metalpa R, Richard C, Allemand D, Bianchi CN, Morri C, Ferrier-Pages C (2006) Response of zooxanthellae in symbiosis with the Mediterranean corals Cladocora caespitosa and Oculina patagonica to elevated temperatures. Mar Biol 150:45–55
Rodolfo-Metalpa R, Hoogenboom MO, Rottier C, Ramos-Esplá A, Baker AC, Fine M, Ferrier-Pagès C (2014) Thermally tolerant corals have limited capacity to acclimatize to future warming. Glob Chang Biol 20:3036–3049
Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326
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
Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269
Rubio-Portillo E, Yarza P, Peñalver C, Ramos-Esplá AA, Antón J (2014a) New insights into Oculina patagonica coral diseases and their associated Vibrio spp. communities. ISME J 8:1794–1807
Rubio-Portillo E, Vázquez-Luis M, Valle C, Izquierdo-Muñoz A, Ramos-Esplá AA (2014b) Growth and bleaching of the coral Oculina patagonica under different environmental conditions in the western Mediterranean Sea. Mar Biol 161:2333–2343
Rubio-Portillo E, Souza-Egipsy V, Ascaso C, de los Rios Murillo A, Ramos-Esplá AA, Antón J (2014c) Eukarya associated with the stony coral Oculina patagonica from the Mediterranean Sea. Mar Genomics 17:17–23
Santos SR, Gutierrez-Rodriguez C, Coffroth MA (2003) Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)—ribosomal DNA sequences. Mar Biotechnol (NY) 5:130–140
Santos SR, Taylor DJ, Kinzie Iii RA, Hidaka M, Sakai K, Coffroth MA (2002) Molecular phylogeny of symbiotic dinoflagellates inferred from partial chloroplast large subunit (23S)-rDNA sequences. Mol Phylogenet Evol 23:97–111
Shenkar N, Fine M, Kramarsky-Winter E, Loya Y (2006) Population dynamics of zooxanthellae during a bacterial bleaching event. Coral Reefs 25:223–227
Stat M, Carter D, Hoegh-Guldberg O (2006) The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspect Plant Ecol Evol Syst 8:23–43
Stat M, Loh WKW, LaJeunesse TC, Hoegh-Guldberg O, Carter DA (2009) Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709–713
Stat M, Pochon X, Franklin EC, Bruno JF, Casey KS, Selig ER, Gates RD (2013) The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress. Ecol Evol 3:1317–1329
Symula RE, Marpuri I, Bjornson RD, Okedi L, Beadell J, Alam U, Aksoy S, Caccone A (2011) Influence of host phylogeographic patterns and incomplete lineage sorting on within-species genetic variability in Wigglesworthia species, obligate symbionts of tsetse flies. Appl Environ Microbiol 77:8400–8408
Szmant A, Gassman N (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224
Tambutté S, Holcomb M, Ferrier-Pagès C, Reynaud S, Tambutté É, Zoccola D, Allemand D (2011) Coral biomineralization: from the gene to the environment. J Exp Mar Biol Ecol 408:58–78
Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535
Thornhill DJ, Fitt WK, Schmidt GW (2006a) Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515–519
Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW (2006b) Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar Biol 148:711–722
Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW (2008) Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbodinium (Dinophyta) lineage. J Phycol 44:1126–1135
Thornhill DJ, Xiang Y, Pettay DT, Zhong M, Santos SR (2013) Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins. Mol Ecol 22:4499–4515
Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biol Bull 201:348–359