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Species richness and generalists–specialists mosaicism of symbiodiniacean symbionts in corals from Hong Kong revealed by high-throughput ITS sequencing

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Abstract

Hong Kong is considered to be a marginal area for coral growth due to its subtropical geography with relatively low winter sea temperatures. Corals can only form non-reefal communities and are believed to host only a low diversity of symbionts with limited flexibility in their symbiont changes. Whether these previously predicted low symbiont diversity is true or is simply a technical artifact and whether these symbionts are generalists or specialists have not fully resolved. To address these issues, we investigated symbiodiniacean diversity and community structure of 30 species of Hong Kong corals using high-throughput sequencing of the nuclear ribosomal RNA gene ITS2. We found high Symbiodiniaceae species richness, with each coral hosting multiple distinct ITS2 symbiont types. Using SymPortal pipeline to alleviate effects of intraspecific ITS polymorphism, the 4662 Symbiodiniaceae ITS2 sequence variants (DIVs) found in our samples were collapsed into 13 distinct ITS2-type profiles, covering Symbiodinium, Breviolum, Cladocopium, and Durusdinium genera, seven of which were coral specific. Cladocopium goreaui was the most diversified (six profiles) and prevalent lineage, dominating the symbiont communities in 29 of the 30 corals species examined. The stress-tolerant Oulastrea crispata was exceptional as its symbionts were dominated by Durusdinium eurythalpos (D13-D13b-D12-D13c profile). Interestingly, Cladocopium C15 was diversified into two ITS2-type profiles, one being Porites lobata specific, while the other was associated with both P. aranetai and P. lutea. Overall, most corals harbor a single dominant generalist symbiont, while some corals host both generalist and specialist symbionts. This work lays the foundation for future research to understand how the generalist and specialist as well as dominant and rare symbionts contribute to the responses and resilience of their host corals against environmental fluctuations in a marginal coral ecosystem, like that in Hong Kong.

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References

  • Ang PO, Ng TY (2018) Updates on the taxonomy of Hong Kong hard Corals: A desktop review. Submitted to Marine Conservation Division, Agriculture, Fisheries and Conservation Department, Hong Kong SAR Government.

  • Ang PO, McCorry D, Choi LS (2003) Establishing a reference collection and field guides for Hong Kong scleractinian coral. Final report. Submitted to Marine Conservation Division, Agriculture, Fisheries and Conservation Department, Hong Kong SAR Government.

  • Ang PO, Choi LS, Choi MM, Cornish A, Fung HL, Lee MW, Lin TP, Ma WC, Tam MC, Wong SY (2005) Hong Kong. In: Status of coral reefs of the East Asian Seas region: 2004. Japan Wildlife Research Centre, Ministry of Environment, Japan, pp 121-152

  • Arif C, Daniels C, Bayer T, Banguera-Hinestroza E, Barbrook A, Howe CJ, Lajeunesse TC, Voolstra CR (2014) Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol Ecol 23:4418–4433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • Baker AC, Romanski AM (2007) Multiple symbiotic partnerships are common in scleractinian corals, but not in octocorals: Comment on Goulet (2006). Mar Ecol Prog Ser 335:237–242

    Article  Google Scholar 

  • Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change: Shifting to new algal symbionts may safeguard devastated reefs from extinction. Nature 430:741

    Article  CAS  PubMed  Google Scholar 

  • Burt JA, Camp EF, Enochs IC, Johansen JL, Morgan KM, Riegl B, Hoe AS (2020) Insights from extreme coral reefs in a changing world. Coral Reefs 39:495–507

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cantin NE, Van Oppen MJH, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405–414

    Article  Google Scholar 

  • Chankong A, Kongjandtre N, Senanan W, Manthachitra V (2020) Community composition of Symbiodiniaceae among four scleractinian corals in the eastern Gulf of Thailand. Reg Stud Mar Sci 33

  • Chen B, Yu K, Liang J, Huang W, Wang G, Roth MS (2019) Latitudinal variation in the molecular diversity and community composition of Symbiodiniaceae in coral from the South China Sea. Front Microbiol 10:1078

    Google Scholar 

  • Claar DC, McDevitt-Irwin JM, Garren M, Vega Thurber R, Gates RD, Baum JK (2020) Increased diversity and concordant shifts in community structure of coral-associated Symbiodiniaceae and bacteria subjected to chronic human disturbance. Mol Ecol 29:2477–2491

    Article  CAS  PubMed  Google Scholar 

  • Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34

    Article  CAS  PubMed  Google Scholar 

  • Correa AMS, McDonald MD, Baker AC (2009) Development of clade-specific Symbiodinium primers for quantitative PCR (qPCR) and their application to detecting clade D symbionts in Caribbean corals. Mar Biol 156:2403–2411

    Article  CAS  Google Scholar 

  • Cunning R, Gates RD, Edmunds PJ (2017) Using high-throughput sequencing of ITS2 to describe Symbiodinium metacommunities in St. John, US Virgin Islands. PeerJ 5:e3472

  • Decelle J, Carradec Q, Pochon X, Henry N, Romac S, Mahé F, Dunthorn M, Kourlaiev A, Voolstra CR, Wincker P, de Vargas C (2018) Worldwide occurrence and activity of the reef-building coral symbiont Symbiodinium in the open ocean. Curr Biol 28:3625–3633

    Article  CAS  PubMed  Google Scholar 

  • Ebenezer V, Medlin LK, Ki JS (2012) Molecular detection, quantification, and diversity evaluation of microalgae. Mar Biotechnol 14(2):129–142

    Article  CAS  Google Scholar 

  • Eckert RJ, Reaume AM, Sturm AB, Studivan MS, Voss JD (2020) Depth Influences Symbiodiniaceae Associations Among Montastraea cavernosa Corals on the Belize Barrier Reef. Front Microbiol 11:518

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong S, Chai G, Xiao Y, Xu L, Yu K, Li J, Liu F, Cheng H, Zhang F, Liao B, Li Z (2018) Flexible symbiotic associations of Symbiodinium with five typical coral species in tropical and subtropical reef regions of the Northern South China Sea. Front Microbiol 9:2485

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong W, Marchetti A (2019) Estimation of 18S gene copy number in marine eukaryotic plankton using a next-generation sequencing approach. Front Mar Sci 6. https://doi.org/10.3389/fmars.2019.00219

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Huang H, Dong ZJ, Huang LM, Yang JH, Di BP, Li YC, Zhou GW, Zhang CL (2011) Latitudinal variation in algal symbionts within the scleractinian coral Galaxea fascicularis in the South China Sea. Mar Biol Res 7:208–211

    Article  Google Scholar 

  • Hume BC, 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 Pollut Bull 72:313–322

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

  • LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581

    Article  CAS  PubMed  Google Scholar 

  • LaJeunesse TC, Loh WKW, Van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054

    Article  Google Scholar 

  • LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • Lee MJ, Jeong HJ, Jang SH, Lee SY, Kang NS, Lee KH, Kim HS, Wham DC, LaJeunesse TC (2016) Most low-abundance “background” Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microb Ecol 71:771–783

    Article  PubMed  Google Scholar 

  • Lewis CL, Neely KL, Rodriguez-Lanetty M (2019) Recurring episodes of thermal stress shift the balance from a dominant host-specialist to a background host-generalist zooxanthella in the threatened pillar coral. Dendrogyra Cylindrus Front Mar Sci 6:5

    Article  Google Scholar 

  • Lin S, Cheng S, Song BB, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang LL, 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

    Article  CAS  PubMed  Google Scholar 

  • Mashini AG, Fard Yazdani M, Ghavam Mostafavi P, Shahhosseiny MH (2017) Analysis of symbiotic Symbiodinium in scleractinian corals off Northwestern Kish Island, Persian Gulf. Mar Ecol 38:1–7

    Article  Google Scholar 

  • Mieog JC, Olsen JL, Berkelmans R, Bleuler-Martinez SA, Willis BL, van Oppen MJH (2009) The roles and interactions of symbiont, host and environment in defining coral fitness. PLoS One 4:e6364

  • Miranda LN, Zhuang Y, Zhang H, Lin S (2012) Phylogenetic analysis guided by intragenomic SSU rDNA polymorphism refines classification of “Alexandrium tamarense” species complex. Harmful Algae 16:35–48

    Article  CAS  Google Scholar 

  • 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 35:939–955

    Article  Google Scholar 

  • Nitschke MR, Craveiro SC, Brandao C, Fidalgo C, Serodio J, Calado AJ, Frommlet JC (2020) Description of Freudenthalidium gen. nov. and Halluxium gen. nov. to formally recognize clades Fr3 and H as genera in the family Symbiodiniaceae (Dinophyceae). J Phycol 56:923–940

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Perry CT, Larcombe P (2003) Marginal and non-reef-building coral environments. Coral Reefs 22:427–432

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pochon X, Pawlowski J (2006) Evolution of the soritids-Symbiodinium symbiosis: a review. Symbiosis 42:77–88

    Google Scholar 

  • Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078

    Article  Google Scholar 

  • Pochon X, Montoya-Burgos JI, Stadelmann B, Pawlowski J (2006) Molecular phylogeny, evolutionary rates, and divergence timing of the symbiotic dinoflagellate genus Symbiodinium. Mol Phylogenet Evol 38:20–30

    Article  CAS  PubMed  Google Scholar 

  • Pochon X, LaJeunesse TC (2021) Miliolidium n. gen, a new symbiodiniacean genus whose members associate with soritid foraminifera or are free‐living. J Eukaryot Microbiol 68: e12856

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

  • Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc Lond B 279:4352–4361

    Google Scholar 

  • Quigley KM, Davies SW, Kenkel CD, Willis BL, Matz M V., Bay LK (2014) Deep-sequencing method for quantifying background abundances of Symbiodinium types: Exploring the rare Symbiodinium biosphere in reef-building corals. PLoS One 9:e94297

  • Reimer JD, Herrera M, Gatins R, Roberts MB, Parkinson JE, Berumen ML (2017) 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 44:661–673

    Article  Google Scholar 

  • Rowan R, Powers DA (1991) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73

    Article  CAS  Google Scholar 

  • Saad OS, Lin X, Ng TY, Li L, Ang P, Lin S (2020) Genome size, rDNA Copy, and qPCR assays for Symbiodiniaceae. Front Microbiol 11:847

    Article  PubMed  PubMed Central  Google Scholar 

  • Sampayo EM, Dove S, Lajeunesse TC (2009) Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol 18:500–519

    Article  CAS  PubMed  Google Scholar 

  • Santos SR, Taylor DJ, Kinzie 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Smith EG, Gurskaya A, Hume BCC, Voolstra CR, Todd PA, Bauman AG, Burt JA (2020) Low Symbiodiniaceae diversity in a turbid marginal reef environment. Coral Reefs 39:545–553

    Article  Google Scholar 

  • Starzak DE, Quinnell RG, Nitschke MR, Davy SK (2014) The influence of symbiont type on photosynthetic carbon flux in a model cnidarian-dinoflagellate symbiosis. Mar Biol 161:711–724

    Article  CAS  Google Scholar 

  • Stat M, Pochon X, Cowie ROM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96

    Article  CAS  Google Scholar 

  • Thompson JN (2009) The Coevolving Web of Life. Am Nat 173:125–140

    Article  PubMed  Google Scholar 

  • Thomson DP, Bearham D, Graham F, Eagle JV (2011) High latitude, deeper water coral bleaching at Rottnest Island. Western Australia Coral Reefs 30:1107

    Article  Google Scholar 

  • Thornhill DJ, Lewis AM, Wham DC, Lajeunesse TC (2014) Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution 68:352–367

    Article  CAS  PubMed  Google Scholar 

  • Tsang RHL, Ang P (2019) Resistance to temperature stress and Drupella corallivory may promote the dominance of Platygyra acuta in the marginal coral communities in Hong Kong. Mar Environ Res 144:20–27

    Article  CAS  PubMed  Google Scholar 

  • Wee HB, Kurihara H, Reimer JD (2019) Reduced Symbiodiniaceae diversity in Palythoa tuberculosa at a heavily acidified coral reef. Coral Reefs 38:311–319

    Article  Google Scholar 

  • Xie JY, Yeung YH, Kwok CK, Kei K, Ang P, Chan LL, Cheang CC, Chow WK, Qiu JW (2020) Localized bleaching and quick recovery in Hong Kong’s coral communities. Mar Pollut Bull 153:1–9

    Article  Google Scholar 

  • Yamashita H, Suzuki G, Hayashibara T, Koike K (2011) Do corals select zooxanthellae by alternative discharge? Mar Biol 158:87–100

    Article  Google Scholar 

  • Yeung CW, Cheang CC, Lee MW, Fung HL, Chow WK, Ang P (2014) Environmental variabilities and the distribution of octocorals and black corals in Hong Kong. Mar Pollut Bull 85:774–782

    Article  CAS  PubMed  Google Scholar 

  • Zhou GW, Huang H (2011) Low genetic diversity of symbiotic dinoflagellates (Symbiodinium) in scleractinian corals from tropical reefs in Southern Hainan Island, China. J Syst Evol 49:598–605

    Article  Google Scholar 

  • Zhou G, Cai L, Li Y, Tong H, Jiang L, Zhang Y et al (2017) Temperature- driven local acclimatization of Symbiodnium hosted by the Coral Galaxea fascicularis at Hainan Island. China Front Microbiol 8:2487

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziegler M, Eguíluz VM, Duarte CM, Voolstra CR (2018) Rare symbionts may contribute to the resilience of coral-algal assemblages. ISME J 12:161–172

    Article  PubMed  Google Scholar 

  • Ziegler M, Roder C, Büchel, C Voolstra CR (2015) Niche acclimatization in Red Sea corals is dependent on flexibility of host-symbiont association. Mar Ecol Prog Ser 533:149-161

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Acknowledgements

We thank Guangzhou Genedenovo Biotechnology Co., Ltd., for help with the bioinformatics analyses. We are grateful to Benjamin Hume from KAUST for generously running SymPortal framework analysis. We thank our reviewers and editor for comments which greatly improved this manuscript. We are indebted to our colleagues in Marine EcoGenomics Laboratory of Xiamen University, China, for generous assistance in this work. This study was supported by National Key Research and Development Program of China Grant 2016YFA0601202 and Fundamental Research Funds for the Central Universities of China Grant 20720180101 (XL).

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SL conceived and supervised the project. SL, OS, LL, and XL designed the study. TN and PA collected and processed the environmental coral samples. OS and XL conducted data analysis. OS carried out the experiments and wrote the first draft of the manuscript. All authors edited and approved the manuscript.

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Correspondence to Xin Lin or Senjie Lin.

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Saad, O.S., Lin, X., Ng, T.Y. et al. Species richness and generalists–specialists mosaicism of symbiodiniacean symbionts in corals from Hong Kong revealed by high-throughput ITS sequencing. Coral Reefs 41, 1–12 (2022). https://doi.org/10.1007/s00338-021-02196-6

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