Abstract
Increased ocean temperatures from anthropogenic climate change induce coral bleaching, the breakdown of symbioses between corals and photosynthetic dinoflagellates. However, some corals thrive in marginal, warm environments that exceed typical bleaching thresholds. Their survival may be mediated by specific genes within the coral host, association with heat-tolerant algal symbionts, and/or distinct bacterial communities. At Mermaid Reef in Great Abaco, The Bahamas, Orbicella faveolata colonies did not bleach during a warming event that reached 33.0 °C, while at Sandy Cay Reef (~ 18 km south), which reached only 32.0 °C, O. faveolata bleached extensively. To investigate abiotic and biotic factors contributing to Mermaid Reef’s higher thermal tolerance, we compared temperature, depth, and coral composition at each site and used microsatellite genotyping, quantitative PCR, and 16S rRNA metabarcoding to examine host genotype diversity, Symbiodiniaceae composition, and bacterial communities in O. faveolata. All O. faveolata colonies at the tolerant Mermaid Reef were clonemates and hosted exclusively Durusdinium symbionts, while colonies at Sandy Cay Reef comprised diverse genotypes and hosted varying proportions of four Symbiodiniaceae genera, which were primarily structured by depth. Mermaid Reef colonies also tended to have higher bacterial family richness than Sandy Cay Reef. These findings suggest that shallow, warm environments like Mermaid Reef may select for few, putatively heat-tolerant genotypes of corals and symbionts, and that while warming may greatly reduce genetic diversity, certain individuals may thrive. Such individuals existing today can provide valuable biological insights and resources for intervention conservation aimed at boosting reef resilience under climate change.
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References
Agisoft LLC (2016) Agisoft PhotoScan user manual. Professional edition, version 1:37
Ahmed HI, Herrera M, Liew YJ, Aranda M (2019) Long-term temperature stress in the coral model Aiptasia Supports the “Anna Karenina Principle” for Bacterial Microbiomes. Front Microbiol 10:975
Amend AS, Barshis DJ, Oliver TA (2012) Coral-associated marine fungi form novel lineages and heterogeneous assemblages. ISME J 6:1291–1301
Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20
Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471
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 110:1387–1392
Baums IB, Devlin-Durante M, Laing BAA, Feingold J, Smith T, Bruckner A, Monteiro J (2014) Marginal coral populations: the densest known aggregation of Pocillopora in the Galápagos Archipelago is of asexual origin. Front Mar Sci 1:59
Bay RA, Palumbi SR (2014) Multilocus Adaptation Associated with Heat Resistance in Reef-Building Corals. Curr Biol 24:2952–2956
Bentis CJ, Kaufman L, Golubic S (2000) Endolithic fungi in reef-building corals (Order: scleractinia) are common, cosmopolitan, and potentially pathogenic. Biol Bull 198:254–260
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 R Soc B 273:2305–2312
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583
Camp EF, Nitschke MR, Rodolfo-Metalpa R, Houlbreque F, Gardner SG, Smith DJ, Zampighi M, Suggett DJ (2017) Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci Rep 7:2434
Carballo-Bolaños R, Denis V, Huang Y-Y, Keshavmurthy S, Chen CA (2019) Temporal variation and photochemical efficiency of species in Symbiodinaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes. PLoS One 14:e0218801
Coles SL (1997) Reef corals occurring in a highly fluctuating temperature environment at Fahal Island, Gulf of Oman (Indian Ocean). Coral Reefs 16:269–272
Coles SL (2003) Coral species diversity and environmental factors in the Arabian Gulf and the Gulf of Oman: a comparison to the Indo-Pacific Region. Atoll Res Bull 507:1–19
Csardi G, Nepusz T (2006) The igraph software package for complex network research. InterJ Complex Syst 1695:1–9
Cunning R (2018) SteponeR: import qPCR data from StepOne Software into R. R package version 0.1.0
Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262
Cunning R, Baker AC (2014) Not just who, but how many: the importance of partner abundance in reef coral symbioses. Front Microbiol 5:400
Cunning R, Ritson-Williams R, Gates RD (2016) Patterns of bleaching and recovery of Montipora capitata in Kāne‘ohe Bay, Hawai‘i, USA. Mar Ecol Prog Ser 551:131–139
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 282:20141725
Davies SW, Rahman M, Meyer E, Green EA, Buschiazzo E, Medina M, Matz MV (2013) Novel polymorphic microsatellite markers for population genetics of the endangered Caribbean star coral, Montastraea faveolata. Mar Biodivers 43:167–172
Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV (2015) Genomic determinants of coral heat tolerance across latitudes. Science 348:1460–1462
Dziedzic KE, Elder H, Tavalire H, Meyer E (2019) Heritable variation in bleaching responses and its functional genomic basis in reef-building corals (Orbicella faveolata). Mol Ecol 28:2238–2253
Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960
Glasl B, Herndl GJ, Frade PR (2016) The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J 10:2280–2292
Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17
Glynn PW, Maté JL, Baker AC, Calderón MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Ni{ñ}o-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez ED, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga NA, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison H, Hobbs JPA, Hoey AS, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
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 Pollut Bull 72:313–322
Innis T, Cunning R, Ritson-Williams R, Wall CB, Gates RD (2018) Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne‘ohe Bay, O‘ahu, Hawai‘i. Coral Reefs 37:423–430
Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162
Jones A, 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
Jones AM, Berkelmans R (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant symbiodinium Type-D. J Mar Biol 2011:
Kahle D, Wickham H (2013) ggmap: spatial Visualization with ggplot2. R J 5:144–161
Kavousi J, Reimer JD, Tanaka Y, Nakamura T (2015) Colony-specific investigations reveal highly variable responses among individual corals to ocean acidification and warming. Mar Environ Res 109:9–20
Kellogg CA (2004) Tropical Archaea: diversity associated with the surface microlayer of corals. Mar Ecol Prog Ser 273:81–88
Kemp DW, Thornhill DJ, Rotjan RD, Iglesias-Prieto R, Fitt WK, Schmidt GW (2015) Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata. Coral Reefs 34:535–547
Kenkel CD, Matz MV (2016) Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat Ecol Evol 1:0014
Kennedy EV, Tonk L, Foster NL, Chollett I, Ortiz JC, Dove SG, Hoegh-Guldberg O, Mumby PJ, Stevens JR (2016) Symbiodinium biogeography tracks environmental patterns rather than host genetics in a key Caribbean reef-builder, Orbicella annularis. Proc R Soc B 283:20161918–20161938
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
Kinsman DJJ (1964) Reef coral tolerance of high temperatures and salinities. Nature 202:1280–1282
LaJeunesse TC, Smith RT, Finney JC, Oxenford HA (2009) Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral “bleaching” event. Proc R Soc B 276:4139–4148
LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010a) Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genusSymbiodinium. J Biogeogr 37:785–800
LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, Pérez AL, Reyes-Bonilla H, Warner ME (2010b) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proc Biol Sci 277:2925–2934
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
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.e6
Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494
McIlroy SE, Cunning R, Baker AC, Coffroth MA (2019) Competition and succession among coral endosymbionts. Ecol Evol 18:3532
McMurdie PJ, Holmes S (2013) phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217
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
Merselis DG, Lirman D, Rodriguez-Lanetty M (2018) Symbiotic immuno-suppression: is disease susceptibility the price of bleaching resistance? PeerJ 6:e4494
Nguyen-Kim H, Bouvier T, Bouvier C, Doan-Nhu H, Nguyen-Ngoc L, Rochelle-Newall E, Baudoux A-C, Desnues C, Reynaud S, Ferrier-Pages C, Bettarel Y (2014) High occurrence of viruses in the mucus layer of scleractinian corals. Environ Microbiol Rep 6:675–682
Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898
Parker KE, Cunning R (2020) Data for: characterization of a thermally tolerant Orbicella faveolata reef in Abaco. The Bahamas Zenodo. https://doi.org/10.5281/zenodo.3827500
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Riegl BM, Purkis SJ, Al-Cibahy AS, Abdel-Moati MA, Hoegh-Guldberg O (2011) Present limits to heat-adaptability in corals and population-level responses to climate extremes. PLoS One 6:e24802
Roder C, Arif C, Daniels C, Weil E, Voolstra CR (2014) Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome. Mol Ecol 23:965–974
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10
Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc Natl Acad Sci U S A 92:2850–2853
Rowan R, Knowlton N, Baker AC, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269
Sacristán-Soriano O, Winkler M, Erwin P, Weisz J, Harriott O, Heussler G, Bauer E, West Marsden B, Hill A, Hill M (2019) Ontogeny of symbiont community structure in two carotenoid-rich, viviparous marine sponges: comparison of microbiomes and analysis of culturable pigmented heterotrophic bacteria. Environ Microbiol Rep 11:249–261
Severance EG, Szmant AM, Karl SA (2004) Single-copy gene markers isolated from the Caribbean coral, Montastraea annularis. Mol Ecol Notes 4:167–169
Sharp KH, Pratte ZA, Kerwin AH, Rotjan RD, Stewart FJ (2017) Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata. Microbiome 5:120
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 21:236–249
van Hooidonk R, Maynard JA, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nat Clim Chang 3:508–511
van Hooidonk R, Maynard JA, Liu Y, Lee S-K (2015) Downscaled projections of Caribbean coral bleaching that can inform conservation planning. Glob Change Biol 21:3389–3401
van Oppen MJH, Blackall LL (2019) Coral microbiome dynamics, functions and design in a changing world. Nat Rev Microbiol 17:557–567
Weiler BA, Verhoeven JTP, Dufour SC (2018) Bacterial Communities in Tissues and Surficial Mucus of the Cold-Water Coral Paragorgia arborea. Frontiers in Marine Science 5:
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer, Berlin
Willis A, Bunge J (2015) Estimating diversity via frequency ratios. Biometrics 71:1042–1049
Willis A, Bunge J, Whitman T (2017) Improved detection of changes in species richness in high diversity microbial communities. J R Stat Soc C 66:963–977
Wilson WH, Dale AL, Davy JE, Davy SK (2005) An enemy within? Observations of virus-like particles in reef corals. Coral Reefs 24:145–148
Zaneveld JR, McMinds R, Thurber RV (2017) Stress and stability: applying the Anna Karenina principle to animal microbiomes. Nat Microbiol 2:17121
Ziegler M, Roik A, Porter A, Zubier K, Mudarris MS, Ormond R, Voolstra CR (2016) Coral microbial community dynamics in response to anthropogenic impacts near a major city in the central Red Sea. Mar Pollut Bull 105:629–640
Ziegler M, Seneca FO, Yum LK, Palumbi SR, Voolstra CR (2017) Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat Commun 8:14213
Acknowledgements
We acknowledge the January 2019 Middlebury College course BIOL0371 Advanced Field Biology, funded by the Middlebury College Biology Department, donors, and the Albert D. Mead Professorship (to JOW), for field support. We also acknowledge the Abaco community that supported our research efforts: DiveTime Abaco, Friends of the Environment, Bahamas National Trust, Mark Grosby, and Island Girl Taxi. Middlebury students from spring 2019 courses BIOL0324 Genomics and BIOL0365 Molecular Microbial Ecology conducted pilot microsatellite analyses, and Will Greene generated the orthomosaic. Margaret Miller provided project support and spawning observations, and Ruben van Hooidonk provided satellite temperature data. Molecular work was supported by the Microbiome Lab at the John G. Shedd Aquarium, the Vermont Integrative Genomics Resource Massively Parallel Sequencing Facility, the University of Vermont Cancer Center, Lake Champlain Cancer Research Organization, and the UVM Larner College of Medicine. KP was supported by NSF OCE-1851305 to RC.
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Symbiodiniaceae qPCR data, environmental data, and R code for analysis are available at github.com/kparker96/Sandy_Mermaid, and are archived at Zenodo (Parker and Cunning 2020). Microbial raw data are available through the NCBI SRA via accession number PRJNA591009, with R code for analysis at github.com/eme47/CoralMicrobiome.
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Parker, K.E., Ward, J.O., Eggleston, E.M. et al. Characterization of a thermally tolerant Orbicella faveolata reef in Abaco, The Bahamas. Coral Reefs 39, 675–685 (2020). https://doi.org/10.1007/s00338-020-01948-0
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DOI: https://doi.org/10.1007/s00338-020-01948-0