Low Symbiodiniaceae diversity in a turbid marginal reef environment

Abstract

The coastal waters of Singapore support coral reefs that are biodiverse but characterized by high turbidity and sedimentation. Here, we used internal transcribed spacer two (ITS2) amplicon sequencing to investigate the Symbiodiniaceae communities associated with this marginal reef system, as turbid reefs may serve as potential refugia from future thermal stress. Using the analytical framework SymPortal, we identified a predominance of Cladocopium among the five coral species studied across six reef sites. Durusdinium was present in comparatively lower abundances and was composed of multiple Durusdinium trenchii strains. In contrast to other marginal environments, the Cladocopium communities exhibited low diversity and lacked the host-specificity of strains reported elsewhere. Nevertheless, we identified a site-specific strain across three species, which was supported by sequencing of the non-coding region of the psbA minicircle (psbAncr). The overall low diversity of the symbiont communities suggests that, although Singapore’s reefs may provide habitat for a diverse coral assemblage, the strong selective pressure exerted by the prevalent turbidity likely limits the diversity of the associated symbiont community.

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References

  1. Anderson MJ, Walsh DC (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574

    Google Scholar 

  2. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJ, 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

    PubMed  PubMed Central  Google Scholar 

  3. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138

    Google Scholar 

  4. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 2:e711

    PubMed  PubMed Central  Google Scholar 

  5. Cacciapaglia C, van Woesik R (2016) Climate-change refugia: shading reef corals by turbidity. Glob Chang Biol 22:1145–1154

    PubMed  Google Scholar 

  6. Camp EF, Schoepf V, Mumby PJ, Hardtke LA, Rodolfo-Metalpa R, Smith DJ, Suggett DJ (2018) The future of coral reefs subject to rapid climate change: lessons from natural extreme environments. Front Mar Sci 5:4

    Google Scholar 

  7. Camp EF, Edmondson J, Doheny A, Rumney J, Grima AJ, Huete A, Suggett DJ (2019) Mangrove lagoons of the Great Barrier Reef support coral populations persisting under extreme environmental conditions. Mar Ecol Prog Ser 625:1–14

    CAS  Google Scholar 

  8. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140

    PubMed  PubMed Central  Google Scholar 

  9. Chia LS, Khan H, Chou LM (1988) The coastal environmental profile of Singapore. WorldFish

  10. D’Angelo C, Hume BC, Burt J, Smith EG, Achterberg EP, Wiedenmann J (2015) Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf. ISME J 9:2551

    PubMed  PubMed Central  Google Scholar 

  11. Dana JD (1846) Zoophytes. In: Wilkes C (ed) United States Exploring Expedition During the years 1838, 1839, 1840, 1841, 1842. Lea and Blanchard, Philadelphia, pp 1–740

  12. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109:17995–17999

    PubMed  Google Scholar 

  13. Dikou A, Van Woesik R (2006) Survival under chronic stress from sediment load: spatial patterns of hard coral communities in the southern islands of Singapore. Mar Pollut Bull 52:1340–1354

    CAS  PubMed  Google Scholar 

  14. Ellis J, Solander DC (1786) The natural history of many curious and uncommon zoophytes: collected from various parts of the globe. Benjamin White and Son, and Peter Elmsly, London

    Google Scholar 

  15. Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH, Sogin ML (2015) Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J 9:968

    CAS  PubMed  Google Scholar 

  16. 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

    CAS  PubMed  Google Scholar 

  17. Glynn PW (1983) Extensive ‘bleaching’and death of reef corals on the Pacific coast of Panama. Environ Conserv 10:149–154

    Google Scholar 

  18. Guest J, Low J, Tun K, Wilson B, Ng C, Raingeard D, Ulstrup K, Tanzil JTI, Todd P, Toh T (2016a) Coral community response to bleaching on a highly disturbed reef. Sci Rep 6:20717

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Guest J, Tun K, Low J, Vergés A, Marzinelli E, Campbell AH, Bauman A, Feary D, Chou L, Steinberg P (2016b) 27 years of benthic and coral community dynamics on turbid, highly urbanised reefs off Singapore. Sci Rep 6:36260

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Hennige SJ, Smith DJ, Walsh S-J, McGinley MP, Warner ME, Suggett DJ (2010) Acclimation and adaptation of scleractinian coral communities along environmental gradients within an Indonesian reef system. J Exp Mar Bio Ecol 391:143–152

    Google Scholar 

  21. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    CAS  PubMed  Google Scholar 

  22. Howells EJ, Abrego D, Meyer E, Kirk NL, Burt JA (2016) Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Glob Chang Biol 22:2702–2714

    PubMed  Google Scholar 

  23. Howells EJ, Bauman AG, Vaughan GO, Hume BC, Voolstra CR, Burt JA (2020) Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Mol Ecol 29:899–911

    CAS  PubMed  Google Scholar 

  24. Huang D, Tun KP, Chou LM, Todd PA (2009) An inventory of zooxanthellate scleractinian corals in Singapore, including 33 new records. Raffles Bulletin of Zoology 22:69–80

    CAS  Google Scholar 

  25. Huang D, Benzoni F, Fukami H, Knowlton N, Smith ND, Budd AF (2014) Taxonomic classification of the reef coral families Merulinidae, Montastraeidae, and Diploastraeidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linn Soc 171:277–355

    Google Scholar 

  26. Hume B, D’angelo C, Burt J, Baker A, 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 Pollut Bull 72:313–322

    CAS  PubMed  Google Scholar 

  27. 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  PubMed  PubMed Central  Google Scholar 

  28. Hume BC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc Natl Acad Sci U S A 113:4416–4421

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Hume BC, D’Angelo C, Burt JA, Wiedenmann J (2018a) Fine-scale biogeographical boundary delineation and sub-population resolution in the Symbiodinium thermophilum coral symbiont group from the Persian/Arabian Gulf and Gulf of Oman. Front Mar Sci 5:138

    Google Scholar 

  30. Hume BC, Ziegler M, Poulain J, Pochon X, Romac S, Boissin E, De Vargas C, Planes S, Wincker P, Voolstra CR (2018b) An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region. PeerJ 6:e4816

    PubMed  PubMed Central  Google Scholar 

  31. Hume BC, Smith EG, Ziegler M, Warrington HJ, Burt JA, LaJeunesse TC, Wiedenmann J, Voolstra CR (2019) SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour 19:1063–1080

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Hume BC, Mejia-Restrepo A, Voolstra CR, Berumen ML (2020) Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs 1–19

  33. Iglesias-Prieto R, Beltran V, Lajeunesse TC, Reyes-Bonilla H, Thome P (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc Biol Sci 271:1757–1763

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 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 Biol Sci 275:1359–1365

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Keshavmurthy S, Meng P-J, Wang J-T, Kuo C-Y, Yang S-Y, Hsu C-M, Gan C-H, Dai C-F, Chen CA (2014) Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input. PeerJ 2:e327

    PubMed  PubMed Central  Google Scholar 

  36. Kleypas JA, McManus JW, Menez LA (1999) Environmental limits to coral reef development: where do we draw the line? Am Zool 39:146–159

    Google Scholar 

  37. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 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:e29013

    CAS  PubMed  PubMed Central  Google Scholar 

  39. LaJeunesse TC, Bonilla HR, Warner M, Wills M, Schmidt G, Fitt W (2008) Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnol Oceanogr 53:719–727

    Google Scholar 

  40. LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53:305–319

    Google Scholar 

  41. 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):e2576

    Google Scholar 

  42. LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, 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 Biogeogr 37:785–800

    Google Scholar 

  43. Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli A (2010) Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: light, food, and genetics. Ecology 91:990–1003

    PubMed  Google Scholar 

  44. Lien Y-T, Nakano Y, Plathong S, Fukami H, Wang J-T, Chen C (2007) Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26:35–44

    Google Scholar 

  45. McGinley MP, Aschaffenburg MD, Pettay DT, Smith RT, LaJeunesse TC, Warner ME (2012) Symbiodinium spp. in colonies of eastern Pacific Pocillopora spp. are highly stable despite the prevalence of low-abundance background populations. Mar Ecol Prog Ser 462:1–7

    Google Scholar 

  46. 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 53:1725–1734

    CAS  PubMed  Google Scholar 

  47. Morgan KM, Perry CT, Johnson JA, Smithers SG (2017) Nearshore turbid-zone corals exhibit high bleaching tolerance on the Great Barrier Reef following the 2016 ocean warming event. Front Mar Sci 4:224

    Google Scholar 

  48. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Google Scholar 

  49. Ng TY, Ang P (2016) Low symbiont diversity as a potential adaptive strategy in a marginal non-reefal environment: a case study of corals in Hong Kong. Coral Reefs 35:941–957

    Google Scholar 

  50. Noda H, Parkinson JE, Yang S-Y, 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

    PubMed  PubMed Central  Google Scholar 

  51. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package. R package version 2.5-6

  52. Oliver T, Palumbi S (2011) Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241–250

    Google Scholar 

  53. Pallas PS (1766) Elenchus zoophytorum sistens generum adumbrationes generaliores et specierum cognitarum… descriptiones etc. Varrentrapp, Den Haag

  54. Poquita-Du RC, Huang D, Chou LM, Todd PA (2020) The contribution of stress-tolerant endosymbiotic dinoflagellate Durusdinium to Pocillopora acuta survival in a highly urbanized reef system. Coral Reefs 1–11

  55. R Core Team (2019) R: A language and environment for statistical computing. Austria, Vienna

    Google Scholar 

  56. Reimer JD, Todd PA (2009) Preliminary molecular examination of zooxanthellate zoanthid (Hexacorallia, Zoantharia) and associated zooxanthellae (Symbiodinium spp.) diversity in Singapore. Raffles Bulletin of Zoology 22:103–120

    Google Scholar 

  57. Ronquist F, Teslenko M, Van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    PubMed  PubMed Central  Google Scholar 

  58. Saville Kent W (1871) On some new and little known species of Madreporaria, or stony corals, in the British Museum collection. Proceedings of the Zoological Society of London 2:275–286

    Google Scholar 

  59. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Smith EG, Vaughan GO, Ketchum RN, McParland D, Burt JA (2017a) Symbiont community stability through severe coral bleaching in a thermally extreme lagoon. Sci Rep 7:2428

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Smith EG, Ketchum RN, Burt JA (2017b) Host specificity of Symbiodinium variants revealed by an ITS2 metahaplotype approach. ISME J 11:1500–1503

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Smith EG, Hume BC, Delaney P, Wiedenmann J, Burt JA (2017c) Genetic structure of coral-Symbiodinium symbioses on the world’s warmest reefs. PLoS ONE 12:e0180169

    PubMed  PubMed Central  Google Scholar 

  63. Smith EG, D’angelo C, Sharon Y, Tchernov D, Wiedenmann J (2017d) Acclimatization of symbiotic corals to mesophotic light environments through wavelength transformation by fluorescent protein pigments. Proc Biol Sci 284:20170320

    PubMed  PubMed Central  Google Scholar 

  64. Stambler N, Dubinsky Z (2005) Corals as light collectors: an integrating sphere approach. Coral Reefs 24:1–9

    Google Scholar 

  65. Tanzil JTI, Ng APK, Tey YQ, Tan BHY, Yun EY, Huang D (2016) A preliminary characterisation of Symbiodinium diversity in some common corals from Singapore. Cosmos 12:15–27

    Google Scholar 

  66. Terraneo TI, Fusi M, Hume BC, Arrigoni R, Voolstra CR, Benzoni F, Forsman ZH, Berumen ML (2019) Environmental latitudinal gradients and host-specificity shape Symbiodiniaceae distribution in Red Sea Porites corals. J Biogeogr 46:2323–2335

    Google Scholar 

  67. Todd PA, Ladle RJ, Lewin-Koh N, Chou LM (2004) Genotype × environment interactions in transplanted clones of the massive corals Favia speciosa and Diploastrea heliopora. Mar Ecol Prog Ser 271:167–182

    Google Scholar 

  68. 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

    CAS  PubMed  Google Scholar 

  69. Veron JE, Stafford-Smith M, Turak E, DeVantier L (2015) Corals of the World (http://www.coralsoftheworld.org/)

  70. Wicks L, Sampayo E, Gardner J, Davy S (2010) Local endemicity and high diversity characterise high-latitude coral–Symbiodinium partnerships. Coral Reefs 29:989–1003

    Google Scholar 

  71. Wilkinson C (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville

    Google Scholar 

  72. Wong JC, Thompson P, Xie JY, Qiu J-W, Baker DM (2016) Symbiodinium clade C generality among common scleractinian corals in subtropical Hong Kong. Reg Stud Mar Sci 8:439–444

    Google Scholar 

  73. Yu G, Smith DK, Zhu H, Guan Y, Lam TTY (2017) GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28–36

    Google Scholar 

  74. 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 44:674–686

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was partially carried out using the Core Technology Platforms resources at New York University Abu Dhabi, including the High Performance Computing Cluster and Sequencing Core Technology Platforms. Collection of coral samples was authorized by Singapore National Parks (NP/RP15-061). We would like to thank the Agri-Food and Veterinary Authority of Singapore for providing CITES export permit 15SG012731CE, and the UAE Ministry of Environment and Climate Change for providing the CITES import permit 15MEW4457. This study was supported by the AXA Fellowship (R-154-000-649-507) to AGB and the National Research Foundation, Prime Minister’s Office, Singapore under the Marine Science Research and Development Programme (R-154-001-A25-281 MSRDP-P03).

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Smith, E.G., Gurskaya, A., Hume, B.C.C. et al. Low Symbiodiniaceae diversity in a turbid marginal reef environment. Coral Reefs 39, 545–553 (2020). https://doi.org/10.1007/s00338-020-01956-0

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Keywords

  • Symbiodiniaceae
  • Marginal reefs
  • ITS2
  • Singapore