Symbiodiniaceae diversity of Palythoa tuberculosa in the central and southern Red Sea influenced by environmental factors

Abstract

Sea surface temperatures (SST) and chlorophyll a concentrations (Chl a) in the southern Red Sea have wide variations based on distance from the coast. To understand how these variations can affect the diversity of symbionts hosted by reef-associated organisms, we conducted a study in the central and southern Red Sea to examine the diversity of Symbiodiniaceae hosted by the zooxanthellate zoantharian Palythoa tuberculosa at different distances from the coast: offshore (FBO), midshelf (FBM) and inshore (FBI) of Farasan Banks, and inshore at Thuwal (TI). Genomic DNA was extracted from 198 specimens, followed by amplification of the ribosomal DNA internal transcribed spacer 2 (ITS-2) and noncoding region of the chloroplast plastid minicircle (psbAncr). Durusdinium and six lineages of Cladocopium (Pt-1-a, Pt-1-b, Pt-1-c, Pt-1-d, Pt-3-a, Pt-3-b) were identified based on sequences of the two marker regions. Changes in composition of Symbiodiniaceae lineages were observed from FBI (high SST, high Chl a) to FBO (low SST, low Chl a). Molecular variance analyses showed that distance from coast was the most likely predictor of differences in Cladocopium lineages. Multinomial logistic regression analysis showed a transition among different Cladocopium lineages as SST increased. One Cladocopium lineage, Pt-1-b, demonstrated higher prevalences at high SSTs and increased in prevalences at the same rate as thermotolerant Durusdinium. Additionally, Cladocopium lineage Pt-3-a had a high affinity to low Chl a concentrations. This study demonstrates that environmental variations in SSTs and Chl a concentrations are significant predictors for the diversity of dominant Symbiodiniaceae within individual host P. tuberculosa colonies. We theorize that flexibility with different lineages of Symbiodiniaceae allows generalist P. tuberculosa to live across a wide range of environments in the southern Red Sea.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Acker JG, Leptoukh G (2007) Online analysis enhances use of NASA earth science data. Eos Trans Am Geophys Union 88(2):14–17

    Article  Google Scholar 

  2. Bailey GN, Flemming NC, King GC, Lambeck K, Momber G, Moran LJ, Al-Sharekh A, Vita-Finzi C (2007) Coastlines, submerged landscapes, and human evolution: the Red Sea Basin and the Farasan Islands. Journal of Island and Coastal Archaeology 2(2):127–160. https://doi.org/10.1080/15564890701623449

    Article  Google Scholar 

  3. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689. https://doi.org/10.1146/132417

    Article  Google Scholar 

  4. Baker DM, Freeman CJ, Wong JC, Fogel ML, Knowlton N (2018) Climate change promotes parasitism in a coral symbiosis. ISME J 12(3):921–930. https://doi.org/10.1038/s41396-018-0046-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Bay LK, Doyle J, Logan M, Berkelmans R (2016) Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. R Soc Open Sci 3(6):160322. https://doi.org/10.1098/rsos.160322

    Article  PubMed  PubMed Central  Google Scholar 

  6. Berumen ML, Hoey AS, Bass WH, Bouwmeester J, Catania D, Cochran JE, Khalil MT, Miyake S, Mughal MR, Spaet JL, Saenz-Agudelo P (2013) The status of coral reef ecology research in the Red Sea. Coral Reefs 32(3):737–748. https://doi.org/10.1007/s00338-013-1055-8

    Article  Google Scholar 

  7. Bongaerts P, Frade PR, Ogier JJ, Hay KB, Van Bleijswijk J, Englebert N, Vermeij MJ, Bak RP, Visser PM, Hoegh-Guldberg O (2013) Sharing the slope: depth partitioning of agariciid corals and associated Symbiodinium across shallow and mesophotic habitats (2–60 m) on a Caribbean reef. BMC Evol Biol 13(1):205. https://doi.org/10.1186/1471-2148-13-205

    Article  PubMed  PubMed Central  Google Scholar 

  8. Brewin RJ, Raitsos DE, Dall’Olmo G, Zarokanellos N, Jackson T, Racault MF, Boss ES, Sathyendranath S, Jones BH, Hoteit I (2015) Regional ocean-colour chlorophyll algorithms for the Red Sea. Remote Sens Environ 165:64–85

    Article  Google Scholar 

  9. Burke L, Reytar KA, Spalding MA, Perr AL (2011) Reefs at risk revisited. World Resources Institute, Washington

    Google Scholar 

  10. Burnett WJ (2002) Longitudinal variation in algal symbionts (zooxanthellae) from the Indian Ocean zoanthid Palythoa caesia. Mar Ecol Prog Ser 234(1991):105–109. https://doi.org/10.3354/meps234105

    Article  Google Scholar 

  11. Caballero I, Stumpf RP, Meredith A (2019) Preliminary assessment of turbidity and chlorophyll impact on bathymetry derived from Sentinel-2A and Sentinel-3A satellites in South Florida. Remote Sens 11(6):645

    Article  Google Scholar 

  12. Chakravarti LJ, Beltran VH, van Oppen MJH (2017) Rapid thermal adaptation in photosymbionts of reef-building corals. Glob Chang Biol 23(11):4675–4688. https://doi.org/10.1111/gcb.13702

    Article  PubMed  Google Scholar 

  13. Cohan FM (2002) What are bacterial species? Annu Rev Microbiol 56(1):457–487

    CAS  Article  Google Scholar 

  14. Coles SL, Bahr KD, Ku’ulei SR, May SL, McGowan AE, Tsang A, Bumgarner J, Han JH (2018) Evidence of acclimatization or adaptation in Hawaiian corals to higher ocean temperatures. PeerJ 6:e5347

    Article  Google Scholar 

  15. Cunning R, Silverstein RN, Baker AC (2015) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc R Soc B Biol Sci 282(1809):20141725

    CAS  Article  Google Scholar 

  16. DiBattista JD, Howard Choat J, Gaither MR, Hobbs JP, Lozano-Cortés DF, Myers RF, Paulay G, Rocha LA, Toonen RJ, Westneat MW, Berumen ML (2016a) On the origin of endemic species in the Red Sea. J Biogeogr 43(1):13–30. https://doi.org/10.1111/jbi.12631

    Article  Google Scholar 

  17. DiBattista JD, Roberts MB, Bouwmeester J, Bowen BW, Coker DJ, Lozano-Cortés DF, Howard Choat J, Gaither MR, Hobbs JP, Khalil MT, Kochzius M (2016b) A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. J Biogeogr 43(3):423–439. https://doi.org/10.1111/jbi.12649

    Article  Google Scholar 

  18. Eladawy A, Nadaoka K, Negm A, Abdel-Fattah S, Hanafy M, Shaltout M (2017) Characterization of the northern Red Sea’s oceanic features with remote sensing data and outputs from a global circulation model. Oceanologia 59(3):213–237. https://doi.org/10.1016/j.oceano.2017.01.002

    Article  Google Scholar 

  19. Fahmy M (2003) Water quality in the Red Sea coastal waters (Egypt): analysis of spatial and temporal variability. Chem Ecol 19(1):67–77

    CAS  Article  Google Scholar 

  20. Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Glob Chang Biol 19(12):3640–3647. https://doi.org/10.1111/gcb.12356

    Article  PubMed  Google Scholar 

  21. Finney JC, Pettay T, Sampayo EM, Warner ME, Oxenford H, LaJeunesse TC (2010) The relative significance of host-habitat, depth, and geography on the ecology, endemism and speciation of coral endosymbionts. Microb Ecol 60:250–263. https://doi.org/10.1007/s00248-010-9681-y

    Article  PubMed  Google Scholar 

  22. Furby KA, Bouwmeester J, Berumen ML (2013) Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 32(2):505–513. https://doi.org/10.1007/s00338-012-0998-5

    Article  Google Scholar 

  23. Grupstra CG, Coma R, Ribes M, Leydet KP, Parkinson JE, McDonald K, Catlla M, Voolstra CR, Hellberg ME, Coffroth MA (2017) Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes. Coral Reefs 36(3):981–985

    Article  Google Scholar 

  24. Hall TA (1999) BioEdit. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  25. Hasegawa M, Kishino H, Yano TA (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22(2):160–174

    CAS  Article  Google Scholar 

  26. Hawkins TD, Hagemeyer JCG, Warner ME (2016) Temperature moderates the infectiousness of two conspecific Symbiodinium strains isolated from the same host population. Environ Microbiol 18(12):5204–5217

    CAS  Article  Google Scholar 

  27. Hibino Y, Todd P, Ashworth CD, Obuchi M, Reimer JD (2013) Monitoring colony colour and zooxanthellae (Symbiodinium spp.) condition in the reef zoanthid Palythoa tuberculosa in Okinawa, Japan. Mar Biol Res 9(8):794–801. https://doi.org/10.1080/17451000.2013.766344

    Article  Google Scholar 

  28. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    CAS  Article  Google Scholar 

  29. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JB, Kleypas J, Lough JM (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301(5635):929–933. https://doi.org/10.1126/science.1085046

    CAS  Article  PubMed  Google Scholar 

  30. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC (2017) Global warming and recurrent mass bleaching of corals. Nature 543(7645):373–377. https://doi.org/10.1038/nature21707

    CAS  Article  PubMed  Google Scholar 

  31. Hume B, D’angelo C, Burt J, Baker AC, Riegl B, Wiedenmann J (2013) Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. Mar Poll Bull 72(2):313–322

    CAS  Article  Google Scholar 

  32. Hume BC, D’Angelo C, Smith EG, Stevens JR, Burt J, Wiedenmann J (2015) Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci Rep 5:8562

    CAS  Article  Google Scholar 

  33. Hunter CL (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. Proc 8th Int Coral Reef Symp (22): 1599–1602

  34. Kemp DW, Cook CB, LaJeunesse TC, Brooks WR (2006) A comparison of the thermal bleaching responses of the zoanthid Palythoa caribaeorum from three geographically different regions in south Florida. J Exp Mar Biol Ecol 335:266–276

    Article  Google Scholar 

  35. Krueger T, Horwitz N, Bodin J, Giovani ME, Escrig S, Meibom A, Fine M (2017) Common reef-building coral in the Northern Red Sea resistant to elevated temperature and acidification. R Soc Open Sci 4(5):170038. https://doi.org/10.1098/rsos.170038

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    CAS  Article  Google Scholar 

  37. Kunihiro S, Reimer JD (2018) Phylogenetic analyses of Symbiodinium isolated from Waminoa and their anthozoan hosts in the Ryukyu Archipelago, southern Japan. Symbiosis 76(3):253–264. https://doi.org/10.1007/s13199-018-0557-0

    Article  Google Scholar 

  38. LaJeunesse TC (2004) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene–Pliocene transition. Mol Biol Evol 22(3):570–581. https://doi.org/10.1093/molbev/msi042

    CAS  Article  PubMed  Google Scholar 

  39. LaJeunesse TC, Thornhill DJ (2011) Improved resolution of reef-coral endosymbiont (Symbiodinium) species diversity, ecology, and evolution through psbA non-coding region genotyping. PLoS One 6(12):e29013. https://doi.org/10.1371/journal.pone.0029013

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. LaJeunesse TC, Bhagooli R, Hidaka M, Done T, deVantier L, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely-related Symbiodinium spp. differ in relative dominance within coral reef host communities across environmental, latitudinal, and biogeographic gradients. Mar Ecol Prog Ser 284:147–161. https://doi.org/10.3354/meps284147

    Article  Google Scholar 

  41. LaJeunesse TC, Pettay T, Sampayo EM, Phongsuwan N, Brown B, Obura D, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeography 37:785–800. https://doi.org/10.1111/j.1365-2699.2010.02273.x

    Article  Google Scholar 

  42. LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress tolerant endosymbionts in the dinoflagellate genus Symbiodinium Clade D are different species. Phycologia 53:305–319. https://doi.org/10.2216/13-186.1

    Article  Google Scholar 

  43. LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580. https://doi.org/10.1016/j.cub.2018.07.008

    CAS  Article  Google Scholar 

  44. Lewis AM, Chan AN, LaJeunesse TC (2019) New species of closely related endosymbiotic dinoflagellates in the greater Caribbean have niches corresponding to host coral phylogeny. J Eukaryot Microbiol 66(3):469–482. https://doi.org/10.1111/jeu.12692

    Article  PubMed  Google Scholar 

  45. Leydet K, Hellberg M (2016) Discordant coral–symbiont structuring: factors shaping geographical variation of Symbiodinium communities in a facultative zooxanthellate coral genus, Oculina. Coral Reefs 35:583–595. https://doi.org/10.1007/s00338-016-1409-0

    Article  Google Scholar 

  46. Lough JM, Anderson KD, Hughes TP (2018) Increasing thermal stress for tropical coral reefs: 1871–2017. Sci Rep 8(1):6079. https://doi.org/10.1038/s41598-018-24530-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Ludt WB, Morgan L, Bishop J, Chakrabarty P (2017) A quantitative and statistical biological comparison of three semi-enclosed seas: The Red Sea, the Persian (Arabian) Gulf, and the Gulf of California. Mar Biodiver 48(4):2119–2124. https://doi.org/10.1007/s12526-017-0740-1

    Article  Google Scholar 

  48. Maynard JA, Anthony KRN, Marshall PA, Masiri I (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar Biol 155(2):173–182

    Article  Google Scholar 

  49. Mies M, Voolstra CR, Castro CB, Pires DO, Calderon EN, Sumida PYG (2017) Expression of a symbiosis-specific gene in Symbiodinium type A1 associated with coral, nudibranch and giant clam larvae. R Soc Open Sci 4(5):170253. https://doi.org/10.1098/rsos.170253

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Monroe AA, Ziegler M, Roik A, Röthig T, Hardenstine RS, Emms MA, Jensen T, Voolstra CR, Berumen ML (2018) In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event. PLoS One 13(4):e0195814. https://doi.org/10.1371/journal.pone.0195814

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Moore RB, Ferguson KM, Loh WK, Hoegh-Guldberg O, Carter DA (2003) Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium. Int J Syst Evol Microbiol 53(6):1725–1734. https://doi.org/10.1099/ijs.0.02594-0

    CAS  Article  PubMed  Google Scholar 

  52. Mostafavi PG, Fatemi SMR, Shahhosseiny MH, Hoegh-Guldberg O, Loh WKW (2007) Predominance of clade D Symbiodinium in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf, Iran). Mar Biol 153(1):25–34

    Article  Google Scholar 

  53. Ngugi DK, Antunes A, Brune A, Stingl U (2012) Biogeography of pelagic bacterioplankton across an antagonistic temperature–salinity gradient in the Red Sea. Mol Ecol 21(2):388–405

    CAS  Article  Google Scholar 

  54. NOAA National Centers for Environmental information, climate at a glance: global time series, published February 2019. Available at: https://www.ncdc.noaa.gov/cag/. Accessed on 27 February 2019

  55. Noda H, Parkinson JE, Yang SY, Reimer JD (2017) A preliminary survey of zoantharian endosymbionts shows high genetic variation over small geographic scales on Okinawa-jima Island, Japan. PeerJ 5:e3740. https://doi.org/10.7717/peerj.3740

    Article  PubMed  PubMed Central  Google Scholar 

  56. Núñez-Pons L, Bertocci I, Baghdasarian G (2017) Symbiont dynamics during thermal acclimation using cnidarian-dinoflagellate model holobionts. Mar Environ Res 130:303–314. https://doi.org/10.1016/j.marenvres.2017.08.005

    CAS  Article  PubMed  Google Scholar 

  57. Oksanen J (2015) Multivariate analysis of ecological communities in R. Available at: http://cc.oulu.fi/~jarioksa/opetus/metodi/vegantutor.pdf. Accessed on 28 February 2019

  58. Osman EO, Smith DJ, Ziegler M, Kürten B, Conrad C, El-Haddad KM, Voolstra CR, Suggett DJ (2017) Thermal refugia against coral bleaching throughout the northern Red Sea. Glob Chang Biol 24(2):e474–484. https://doi.org/10.1111/gcb.13895

    Article  PubMed  Google Scholar 

  59. Otero E, Carbery KK (2005) Chlorophyll a and turbidity patterns over coral reefs systems of La Parguera Natural Reserve, Puerto Rico. Rev Biol Trop 53:25–32

    PubMed  Google Scholar 

  60. Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ 2:e394. https://doi.org/10.7717/peerj.394

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. QGIS Development Team (2019) QGIS geographic information system. Open Source Geospatial Foundation Project. http://qgis.osgeo.org

  62. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  63. Raitsos DE, Pradhan Y, Brewin RJW, Stenchikov G, Hoteit I (2013) Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS One 8(6):e64909. https://doi.org/10.1371/journal.pone.0064909

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Raymundo LJ, Couch CS, Harvell CD, Raymundo J, Bruckner AW, Work TM, Weil E, Woodley CM, Jordan-Dahlgren E, Willis BL, Sato Y (2008) Coral disease handbook guidelines for assessment, monitoring & management

  65. Reimer JD, Todd PA (2009) Preliminary molecular examination of zooxanthellate zoanthids (Hexacorallia: Zoantharia) and associated zooxanthellae (Symbiodinium spp.) diversity in Singapore. Raffles Bull Zool 22:103–120

    Google Scholar 

  66. Reimer JD, Takishita K, Ono S, Maruyama T, Tsukahara J (2006) Latitudinal and intracolony ITS-rDNA sequence variation in the symbiotic dinoflagellate genus Symbiodinium (Dinophyceae) in Zoanthus sansibaricus (Anthozoa: Hexacorallia). Phycol Res 54(2):122–132. https://doi.org/10.1111/j.1440-1835.2006.00419.x

    CAS  Article  Google Scholar 

  67. Reimer JD, Herrera M, Gatins R, Roberts MB, Parkinson JE, Berumen ML (2017a) Latitudinal variation in the symbiotic dinoflagellate Symbiodinium of the common reef zoantharian Palythoa tuberculosa on the Saudi Arabian coast of the Red Sea. J Biogeogr 44(3):661–673. https://doi.org/10.1111/jbi.12795

    Article  Google Scholar 

  68. Reimer JD, Montenegro J, Santos ME, Low ME, Herrera M, Gatins R, Roberts MB, Berumen ML (2017b) Zooxanthellate zoantharians (Anthozoa: Hexacorallia: Zoantharia: Brachycnemina) in the northern Red Sea. Mar Biodivers 47(4):1079–1091. https://doi.org/10.1007/s12526-017-0706-3

    Article  Google Scholar 

  69. Ripley B, Venables W (2016) Feed-forward neural networks and multinomial log-linear models. CRAN. Available at: https://docs.google.com/viewer?url=https%3A%2F%2Fcran.r-project.org%2Fweb%2Fpackages%2Fnnet%2Fnnet.pdf. Accessed on 28 February 2019

  70. Roik A, Roder C, Röthig T, Voolstra CR (2016) Spatial and seasonal reef calcification in corals and calcareous crusts in the central Red Sea. Coral Reefs 35(2):681–693

    Article  Google Scholar 

  71. Rowan R, Powers D (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71(1):65–73. https://doi.org/10.3354/meps071065

    CAS  Article  Google Scholar 

  72. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S (2007) Niche partitioning of closely related symbiotic dinoflagellates. Mol Ecol 16(17):3721–3733. https://doi.org/10.1111/j.1365-294X.2007.03403.x

    CAS  Article  PubMed  Google Scholar 

  73. Sampayo EM, Dove S, Lajeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18(3):500–519. https://doi.org/10.1111/j.1365-294X.2008.04037.x

    CAS  Article  PubMed  Google Scholar 

  74. Sawall Y, Al-Sofyani A, Banguera-Hinestroza E, Voolstra CR (2014) Spatio-temporal analyses of Symbiodinium physiology of the coral Pocillopora verrucosa along large-scale nutrient and temperature gradients in the Red Sea. PloS One 9(8):e103179

    Article  Google Scholar 

  75. Silverstein RN, Cunning R, Baker AC (2015) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Chang Biol 21(1):236–249. https://doi.org/10.1111/gcb.12706

    Article  PubMed  Google Scholar 

  76. Silverstein RN, Cunning R, Baker AC (2017) Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment. J Exp Biol 220(7):1192–1196. https://doi.org/10.1242/jeb.148239

    Article  PubMed  Google Scholar 

  77. Smith EG, Hume BC, Delaney P, Wiedenmann J, Burt JA (2017a) Genetic structure of coral-Symbiodinium symbioses on the world’s warmest reefs. PLoS One 12(6): 1–12. e0180169 https://doi.org/10.1371/journal.pone.0180169

  78. Smith EG, Ketchum RN, Burt JA (2017b) Host specificity of Symbiodinium variants revealed by an ITS2 metahaplotype approach. ISME J 11(6):1500–1503. https://doi.org/10.1038/ismej.2016.206

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  79. Sofianos SS, Johns WE (2003) An oceanic general circulation model (OGCM) investigation of the Red Sea circulation: 2. Three-dimensional circulation in the Red Sea. J Geophys Res Oceans 108(C3)

  80. Sonnewald M, El-Sherbiny MM (2017) Editorial: Red Sea biodiversity. Mar Biodivers 47(4):991–993. https://doi.org/10.1007/s12526-017-0648-9

    Article  Google Scholar 

  81. Thornhill DJ, Lewis AM, Wham DC, LaJeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evol 68(2):352–367. https://doi.org/10.1111/evo.12270

    CAS  Article  Google Scholar 

  82. Thornhill DJ, Howells EJ, Wham DC, Steury TD, Santos SR (2017) Population genetics of reef coral endosymbionts (Symbiodinium, Dinophyceae). Mol Ecol 26(10):2640–2659. https://doi.org/10.1111/mec.14055

    CAS  Article  PubMed  Google Scholar 

  83. Tonk L, Sampayo EM, Weeks S, Magno-Canto M, Hoegh-Guldberg O (2013) Host-specific interactions with environmental factors shape the distribution of Symbiodinium across the Great Barrier Reef. PLoS One 8(7):e68533. https://doi.org/10.1371/journal.pone.0068533

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  84. Wee HB, Kurihara H, Reimer JD (2019) Reduced Symbiodiniaceae diversity in Palythoa tuberculosa at a heavily acidified coral reef. Coral Reefs 38(2):311–319. https://doi.org/10.1007/s00338-019-01776-x

    Article  Google Scholar 

  85. White TJ, Bruns T, Lee SJWT, Taylor JL (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications 18(1):315–322

    Google Scholar 

  86. Wong JC, Thompson P, Xie JY, Qiu JW, Baker DM (2016) Symbiodinium clade C generality among common Scleractinian corals in subtropical Hong Kong. Reg Stud Mar Sci 8(1):439–444

    Article  Google Scholar 

  87. Yao F, Hoteit I, Pratt LJ, Bower AS, Zhai P, Köhl A, Gopalakrishnan G (2014) Seasonal overturning circulation in the Red Sea: 1. Model validation and summer circulation. JGR: Oceans 119(4):2238–2262

    Google Scholar 

  88. Yee TW (2015) Vector generalized linear and additive models: with an implementation in {R}. Springer, New York

    Book  Google Scholar 

  89. Zhu T, Shen S, Acker J, Leptoukh G, Kempler S (2007) Remotely-sensed chlorophyll a observations of the northern Red Sea indicate seasonal variability and influence of coastal reefs. J Mar Syst 69(3–4):191–204. https://doi.org/10.1016/j.jmarsys.2005.12.006

    Article  Google Scholar 

  90. Ziegler M, Arif C, Burt JA, Dobretsov S, Roder C, LaJeunesse TC, Voolstra CR (2017) Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula. J Biogeogr 44(3):674–686. https://doi.org/10.1111/jbi.12913

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was partially funded by the King Abdullah University of Science and Technology (KAUST) (award URF/1/1389-01-01, Red Sea Research Center funds, and baseline research funds to MLB and TR), JSPS Kakenhi-Kiban B grant entitled “Global evolution of Brachycnemina and their Symbiodinium” to JDR, and Sasagawa Research Foundation funding to HBW (29-751). We wish to thank the captain and crew of the MV Dream Master, the KAUST Coastal and Marine Resources Core Laboratory, A. Gusti (KAUST), Roberto Arrigoni, Darren Coker, Tane Sinclair-Taylor and other members of the KAUST Reef Ecology Lab for fieldwork assistance in the Red Sea. Comments from two reviewers greatly improved an earlier version of this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hin Boo Wee.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topic Editor Morgan S. Pratchett

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 101 kb)

Supplementary material 2 (FAS 31 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wee, H.B., Berumen, M.L., Ravasi, T. et al. Symbiodiniaceae diversity of Palythoa tuberculosa in the central and southern Red Sea influenced by environmental factors. Coral Reefs 39, 1619–1633 (2020). https://doi.org/10.1007/s00338-020-01989-5

Download citation

Keywords

  • Saudi Arabia
  • Zooxanthellae
  • Zoantharian
  • Sea surface temperature
  • Chlorophyll a