Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The contribution of stress-tolerant endosymbiotic dinoflagellate Durusdinium to Pocillopora acuta survival in a highly urbanized reef system


Urban coral reefs are regarded as marginal communities that live under localized conditions considered detrimental for coral survival, such as high sediment load. They are also impacted by global environmental changes, especially increases in sea surface temperatures. These conditions can cause sub-optimal performance and may lead to dissociation of the mutualistic symbiosis between the coral host and its endosymbionts (Symbiodiniaceae), which provide the majority of the coral’s daily energy budget. While recent studies have explored gene transcriptional responses to extreme conditions using cultured cells of Symbiodiniaceae, it is generally unknown how their responses manifest in hospite. Here, we investigate differential gene expression of endosymbionts hosted by the common reef-building coral Pocillopora acuta, following separate and combined exposures to two major environmental stressors: heat and sediment. We report that Durusdinium largely dominate the Symbiodiniaceae population in P. acuta, which suggests that the observed differential gene expression patterns are mainly responses from this known stress-tolerant endosymbiont genus. Differentially expressed genes were detected in response to heat, and to combined heat and sediment. These genes are associated with various biological processes including apoptosis, cell proliferation, cell–extracellular matrix adhesion, DNA damage repair, lipid catabolism, and lipid homeostasis. Our study provides valuable insights regarding the role of gene regulation by the endosymbiotic dinoflagellates to help maintain health and function of the coral host, which ultimately contributes to the persistence of P. acuta in Singapore’s highly urbanized reefs.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

Data availability

The datasets generated and/or analyzed during the current study are available at Zenodo (https://doi.org/10.5281/zenodo.3514687).


  1. Allemand D, Tambuttè É, Zoccola D, Tambuttè S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 119–150

  2. Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Baijic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep 6:39734

  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

  4. Baker AC (2004) Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. In: Rosenberg E, Loya Y (eds) Coral health and diseases, vol 8. Springer, Berlin, pp 177–194

  5. Baker DM, Freeman CJ, Wong JCY, Fogel ML, Knowlton N (2018) Climate change promotes parasitism in a coral symbiosis. ISME J 12:921–930

  6. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proc Natl Acad Sci USA 110(4):1387–1392

  7. Barshis DJ, Ladner JT, Oliver TA, Palumbi SR (2014) Lineage-specific transcriptional profiles of Symbiodinium spp. unaltered by heat stress in a coral host. Mol Biol Evol 31:1343–1352

  8. Bellantuono AJ, Dougan KE, Granados-Cifuentes C, Rodriguez-Lanetty M (2019) Transcriptome landscape of a thermal-tolerant coral endosymbiont reveals molecular signature of symbiosis and dysbiosis. BioRxiv. https://doi.org/10.1101/508184

  9. 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 Biol Sci 273:2305–2312

  10. Brian JI, Davy SK, Wilkinson SP (2019) Elevated Symbiodiniaceae richness at Atauro Island (Timor-Leste): a highly biodiverse reef system. Coral Reefs 38(1):123–136

  11. Browne NK, Precht E, Last KS, Todd PA (2014) Photo-physiological costs associated with acute sediment stress events in three near-shore turbid water corals. Mar Ecol Prog Ser 502:129–143

  12. Cavalier-Smith T (1978) The evolutionary origin and phylogeny of microtubules, mitotic spindles and eukaryotic flagella. Biosystems 10:93–114

  13. Cavalier-Smith T (1986) The kingdom Chromista: origin and systematics. In: Round FE, Chapman DJ (eds) Progress in phycological research. Biopress, Bristol, pp 309–347

  14. Chou LM (1996) Response of Singapore reefs to land reclamation. Galaxea 13:85–92

  15. Chou LM, Toh TC, Toh KB, Ng CSL, Cabaitan PC, Tun K, Goh E, Afiq-Rosli L, Taira D, Poquita-Du RC, Loke HX, Khalis A, Li J, Song T (2016) Differential response of coral assemblages to thermal stress underscores the complexity in predicting bleaching sausceptibility. PLoS One 11:e0159755

  16. Chow GSE, Chan YKS, Jain SS, Huang D (2019) Light limitation selects for depth generalists in urbanised reef coral communities. Mar Environ Res 147:101–112

  17. Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. Rev Mineral Geochem 54:151–187

  18. Cooper TF, Berkelmans R, Ulstrup KE, Weeks S, Radford B, Jones AM, Doyle J, Canto M, O’Leary RA, Van Oppen MJ (2011) Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLoS One 6:e25536

  19. Cunning R, Baker AC (2014) Not just who, but how many: the importance of partner abundance in reef coral symbioses. Front Microbiol 5:400

  20. Cunning R, Gillette P, Capo T, Galvez K, Baker AC (2015) Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans. Coral Reefs 34:155–160

  21. Davies SW, Ries JB, Marchetti A, Castillo KD (2018) Symbiodinium functional diversity in the coral Sideastrea siderea is influenced by thermal stress and reef environment, but not ocean acidification. Front Mar Sci 5:150

  22. Davies SW, Wham DC, Kanke MR, Matz MV (2019) Contrasting population genetic structure in Acropora coral hosts and their algal symbionts across multiple spatial scales. BioRxiv. https://doi.org/10.1101/575183

  23. 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 U S A 109:17995–17999

  24. Erftemeijer PLA, Riegl B, Hoeksema BW, Todd PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: a review. Mar Pollut Bull 64(9):1737–1765

  25. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJ (2004) Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol Ecol 13:2445–2458

  26. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709

  27. Finney J, Pettay D, Sampayo E, Warner M, Oxenford H, LaJeunesse T (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

  28. Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65

  29. Gierz SL, Foret S, Leggat W (2017) Transcriptomic analysis of thermally stressed Symbiodinium reveals differential expression of stress and metabolism genes. Front Plant Sci 8:271

  30. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7(3):e33353

  31. Guest JR, Low J, Tun K, Wilson B, Ng C, Raingeard D, Ulstrup KE, Tanzil JT, Todd PA, McDougald D, Chou LM, Steinberg PD (2016) Coral community response to bleaching on a highly disturbed reef. Sci Rep 15:6

  32. Heery EC, Hoeksema BW, Browne NK, Reimer JD, Ang PO, Huang D, Friess DA, Chou LM, Loke LHL, Saksena-Taylor P, Alsagoff N, Yeemin T, Sutthacheep M, Vo ST, Bos AR, Gumanao GS, Syed Hussein MA, Waheed Z, Lane DJW, Johan O, Kunzmann A, Jompa J, Suharsono Taira D, Bauman AG, Todd PA (2018) Urban coral reefs: degradation and resilience of hard coral assemblages in coastal cities of East and Southeast Asia. Mar Pollut Bull 135:654–681

  33. Helman Y, Natale F, Sherrell RM, LaVigne M, Starovoytov V, Gorbunov MY, Falkowski PG (2008) Extracellular matrix production and calcium carbonate precipitation by coral cells in vitro. Proc Natl Acad Sci U S A 105:54–58

  34. Hilton MJ, Manning SS (1995) Conversion of coastal habitats in Singapore: indications of unsustainable development. Environ Conserv 22:307–322

  35. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

  36. Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH (2012) Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang 2:116–120

  37. Huang D, Tun KPP, Chou LM, Todd PA (2009) An inventory of zooxanthellate scleractinian corals in Singapore including 33 new records. Raffles Bull Zool S22:69–80

  38. Hume B, D’Angelo C, Burt J, Baker AC, Riegl BM, 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

  39. Hume BCC, 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(16):4416–4421

  40. Jones AM, Berkelmans R (2010) Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS ONE 5:e10437

  41. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field of evidence of acclimatization. Proc R Soc B Biol Sci 275:1359–1365

  42. Kasuba KC, Vavilala SL, D’Souza JS (2015) Apoptosis-like cell death in unicellular photosynthetic organisms—a review. Algal Res 12:126–133

  43. Kramer RH, Marks N (1989) Identification of integrin collagen receptors on human melanoma cells. J Biol Chem 264:4684–4688

  44. Kvitt H, Rosenfeld H, Tchernov D (2016) The regulation of thermal stress induced apoptosis in corals reveals high similarities in gene expression and function to higher animals. Sci Rep 6:30359

  45. Kvitt H, Rosenfeld H, Zandbank K, Tchernov D (2011) Regulation of apoptotic pathways by Stylophora pistillata (Anthozoa, Pocilloporidae) to survive thermal stress and bleaching. PLoS ONE 6:e28665

  46. Lai S, Loke LHL, Hilton MJ, Bouma TJ, Todd PA (2015) The effects of urbanisation on coastal habitats and the potential for ecological engineering: a Singapore case study. Ocean Coast Manag 103:78–85

  47. LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny endosymbiotic dinoflagellates in the genus Symbiodinium using the internal transcribed spacer region: in search of a “species” level marker. J Phycol 37:866–880

  48. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

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

  50. 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(16):2570–2580

  51. 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

  52. 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

  53. Lee RE, Kugrens P (1992) Relationship between the flagellates and the ciliates. Microbiol Rev 56:529–542

  54. Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, pp 405–419

  55. Levin RA, Beltran VH, Hill R, Kjelleberg S, McDougald D, Steinberg PD, van Oppen MJ (2016) Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Mol Biol Evol 33:2201–2215

  56. Leveque S, Afiq-Rosli L, Ip YCA, Jain SS, Huang D (2019) Searching for phylogenetic patterns of Symbiodiniaceae community structure among Indo-Pacific Merulinidae corals. PeerJ 7:e7669. https://doi.org/10.7717/peerj.7669

  57. Lien YT, Nakano Y, Plathong S, Fukami H, Wang JT, Chen CA (2007) Occurrence of putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26(1):35–44

  58. Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wang Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell DA, Sturm NR, Dagenais-Bellefeuille S, Morse D (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350:691–694

  59. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

  60. Malicki JJ, Johnson CA (2017) The cilium: cellular antenna and central processing unit. Trends Cell Biol 27:126–140

  61. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056

  62. Mitchell DR (2007) The evolution of eukaryotic cilia and flagella as motile and sensory organelles. In: Jekely G (ed) Eukaryotic membranes and cytoskeleton advances in experimental medicine and biology, vol 607. Springer, New York, pp 130–140

  63. Mohamed AR, Andrade N, Moya A, Chan CX, Negri AP, Bourne DG, Ball EE, Miller DJ (2019) Transcriptomic insights into the establishment of coral-algal symbioses from the symbiont perspective. BioRxiv. https://doi.org/10.1101/652131

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

  65. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56(1):492–497

  66. Pochon X, Putnam HM, Gates RD (2014) Multi-gene analysis of Symbiodinium dinoflagellates: a perspective on rarity, symbiosis, and evolution. PeerJ 2:e394

  67. Poquita-Du RC, Ng CSL, Loo JB, Afiq-Rosli L, Tay YC, Todd PA, Chou LM, Huang D (2017) New evidence shows that Pocillopora ‘‘damicornis-like’’ corals in Singapore are actually Pocillopora acuta (Scleractinia: Pocilloporidae). Biodivers Data J 5:e11407

  68. Poquita-Du RC, Huang D, Chou LM, Mrinalini Todd PA (2019a) Short term exposure to heat and sediment triggers changes in coral gene expression and photo-physiological performance. Front Mar Sci 6:121

  69. Poquita-Du RC, Quek ZBR, Jain SS, Schmidt-Roach S, Tun K, Heery EC, Chou LM, Todd PA, Huang D (2019b) Last species standing: loss of Pocilloporidae corals associated with coastal urbanization in a tropical city state. Mar Biodivers 49(4):1727–1741

  70. Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc Biol Sci 279(1746):4352–4361

  71. Radakovits R, Jinkerson RE, Darzins A, Posewitz MC (2010) Genetic engineering of algae for enhanced biofuel production. Eukaryot Cell 9:485–501

  72. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

  73. Robinson MD, Smyth GK (2008) Small-sample estimation of negative binomial dispersion, with applications to sage data. Biostatistics 9:321–332

  74. Rouzé H, Lecellier GJ, Saulnier D, Planes S, Gueguen Y, Wirshing HH, Berteaux-Lecellier V (2017) An updated assessment of Symbiodinium spp. that associate with common scleractinian corals from Moorea (French Polynesia) reveals high diversity among background symbionts and a novel finding of clade B. PeerJ 5:e2856

  75. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci U S A 92:2850–2853

  76. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449

  77. Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdae S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Battacharya D, Satoh N (2013) Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol 23(15):1399–1408

  78. Shoguchi E, Beedessee G, Tada I, Hisata K, Kawashima T, Takeuchi T, Arakaki N, Fujie M, Koyanagi R, Roy MC, Kawachi M, Hidaka M, Satoh N, Shinzato C (2018) Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes. BMC Genomics 19:458

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

  80. Stat M, Gates RD (2011) Clade D Symbiodinium in scleractinian corals: a ‘nugget’ of hope, a selfish opportunist, an ominous sign, or all of the above? J Mar Biol 2011:730715

  81. Taira D, Toh TC, Ng CSL, Loke HX, Afiq-Rosli L, Cabaitan PC, Toh KB, Poquita-Du RC, Chou LM, Song T (2017) Relocating bleached Platygyra sinensis facilitates recovery from thermal stress during a minor bleaching event. Mar Freshw Behav Physiol 50:375–385

  82. Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164

  83. Takada Y, Wayner EA, Carter WG, Hemler ME (1988) Extracellular matrix receptors, ECMRII and ECMRI, for collagen and fibronectin correspond to VLA-2 and VLA-3 in the VLA family of heterodimers. J Cell Biochem 37:385–393

  84. Tan KWM, Lee YK (2016) The dilemma for lipid productivity in green microalgae: importance of substrate provision in improving oil yield without sacrificing growth. Biotechnol Biofuels 9:255

  85. Thornhill DJ, Xiang Y, Fitt WK, Santos SR (2009) Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS One 4(7):e6262

  86. Todd PA, Ong X, Chou LM (2010) Impacts of pollution on marine life in Southeast Asia. Biodivers Conserv 19:1063–1082

  87. Toh TC, Huang D, Tun K, Chou LM (2018) Summary of coral bleaching from 2014 to 2017 in Singapore. In: Kimura T, Tun K, Chou LM (eds) Status of coral reefs in East Asian Seas Region: 2018. Ministry of the Environment of Japan and Japan Wildlife Research, Tokyo, pp 21–23

  88. Trench RK, Colley NJ, Fitt WK (1981) Recognition phenomena in symbioses between marine invertebrates and “zooxanthellae”; uptake, sequestration and persistence. Ber Deutsch Bot Ges Bd 94:529–545

  89. Tukwell D, Calderwood DA, Green LJ, Humphries MJ (1995) Integrin α2 I-domain is a binding site for collagens. J Cell Sci 108:1629–1637

  90. Tun KPP (2012) Optimisation of reef survey methods and application of reef metrics and biocriteria for the monitoring of sediment-impacted reefs. Ph.D. thesis, National University of Singapore, p 29

  91. Ulstrup KE, van Oppen MJH (2003) Geographic and habit partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol Ecol 12:3477–3484

  92. van Oppen MJH, Mahiny AJ, Done TJ (2005) Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24(3):482–487

  93. Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ 19:291–299

  94. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066

  95. Wong JSY, Chan YKS, Ng CSL, Tun KPP, Darling ES, Huang D (2018) Comparing patterns of taxonomic, functional and phylogenetic diversity in reef coral communities. Coral Reefs 37:737–750

  96. Yonge CM (1968) Review lecture: living corals. Proc R Soc Lond B Biol Sci 169:329–344

  97. Yonge CM, Nicholls AG, Yonge MJ (1932) The relationship between respiration in corals and the production of oxygen by their zooxanthellae. Sci Rep Great Barrier Reef Exped 1:213–251

  98. Zhang H, Bhattacharya D, Lin S (2005) Phylogeny of dinoflagellates based on mitochondrial cytochrome b and nuclear small subunit rDNA sequence comparisons. J Phycol 41:411–420

Download references


This work was supported by the National Research Foundation, Prime Minister’s Office, Singapore, under its Marine Science Research and Development Program (Award Nos. MSRDP-P03 and No. MSRDP-P05).

Author information

RCPD, DH, CLM, and PAT contributed to conception and design of the study; RCPD carried out the experiment, organized the data, and performed bioinformatics for differential gene expression analysis and functional profiling. All authors contributed to manuscript revision, read, and approved the submitted version.

Correspondence to Rosa Celia Poquita-Du.

Ethics declarations

Conflict of interest

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 Emma Camp

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Poquita-Du, R.C., Huang, D., Chou, L.M. et al. The contribution of stress-tolerant endosymbiotic dinoflagellate Durusdinium to Pocillopora acuta survival in a highly urbanized reef system. Coral Reefs (2020). https://doi.org/10.1007/s00338-020-01902-0

Download citation


  • Endosymbionts
  • Functional profiling
  • Gene expression
  • Holobiont
  • RNA-Seq
  • Symbiodiniaceae