The symbiosis between scleractinian corals and photosynthetic algae from the family Symbiodiniaceae underpins the health and productivity of tropical coral reef ecosystems. While this photosymbiotic association has been extensively studied in shallow waters (<30 m depth), we do not know how deeper corals, inhabiting large and vastly underexplored mesophotic coral ecosystems, modulate their symbiotic associations to grow in environments that receive less than 1% of surface irradiance. Here we report on the deepest photosymbiotic scleractinian corals collected to date (172 m depth), and use amplicon sequencing to identify the associated symbiotic communities. The corals, identified as Leptoseris hawaiiensis, were confirmed to host Symbiodiniaceae, predominantly of the genus Cladocopium, a single species of endolithic algae from the genus Ostreobium, and diverse communities of prokaryotes. Our results expand the reported depth range of photosynthetic scleractinian corals (0–172 m depth), and provide new insights on their symbiotic associations at the lower depth extremes of tropical coral reefs.
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Blackall LL, Wilson B, Van Oppen MJH. Coral—the world’s most diverse symbiotic ecosystem. Mol Ecol. 2015;24:5330–5347.
Pearse V, Muscatine L. Role of symbiotic algae (zooxanthellae) in coral calcification. Biol Bull. 1971;141:350–363.
Muscatine L, Porter JW. Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience. 1977;27:454–460.
Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, et al. Community ecology of mesophotic coral reef ecosystems. Coral Reefs. 2010;29:255–275.
Maragos JE, Jokiel PL. Reef corals of Johnston Atoll: one of the world’s most isolated reefs. Coral Reefs. 1986;4:141–150.
Gattuso JP, Gentili B, Duarte CM, Kleypas JA, Middelburg JJ, Antoine D. Light availability in the coastal ocean: Impact on the distribution of benthic photosynthetic organisms and their contribution to primary production. Biogeosciences. 2006;3:489–513.
Wagner D, Pochon X, Irwin L, Toonen RJ, Gates RD. Azooxanthellate? Most Hawaiian black corals contain Symbiodinium. Proc R Soc B Biol Sci. 2011;278:1323–1328.
Bongaerts P, Sampayo EM, Bridge TCL, Ridgway T, Vermeulen F, Englebert N, et al. Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment. Mar Ecol Prog Ser. 2011;439:117–126.
Padilla-Gamiño JL, Roth MS, Rodrigues LJ, Bradley CJ, Bidigare RR, Gates RD, et al. Ecophysiology of mesophotic reef-building corals in Hawai’i is influenced by symbiont–host associations, photoacclimatization, trophic plasticity, and adaptation. Limnol Oceanogr. 2019;64:1980–1995.
Pochon X, Forsman Z, Spalding H, Padilla-Gamiño J, Smith C, Gates R. Depth specialization in mesophotic corals (Leptoseris spp.) and associated algal symbionts in Hawaii. R Soc Open Sci. 2015;2:140351.
Chan YL, Pochon X, Fisher MA, Wagner D, Concepcion GT, Kahng SE, et al. Generalist dinoflagellate endosymbionts and host genotype diversity detected from mesophotic (67–100 m depths) coral Leptoseris. BMC Ecol. 2009;9:21.
Thornhill DJ, Lewis AM, Wham DC, Lajeunesse TC. Host-specialist lineages dominate the adaptive radiation of reef coral endosymbionts. Evolution. 2014;68:352–367.
Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD. GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium-host symbioses. Mol Ecol Resour. 2012;12:369–373.
Ziegler M, Roder CM, Büchel C, Voolstra CR. Mesophotic coral depth acclimatization is a function of host-specific symbiont physiology. Front Mar Sci. 2015;2:4.
Polinski JM, Voss JD. Evidence of photoacclimatization at mesophotic depths in the coral-Symbiodinium symbiosis at Flower Garden Banks National Marine Sanctuary and McGrail Bank. Coral Reefs. 2018;37:779–789.
Hume BCC, Smith EG, Ziegler M, Warrington HJM, Burt JA, LaJeunesse TC, et al. SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol Ecol Resour. 2019;19:1063–1080.
Pettay D, Wham D, Smith R, Iglesias-Prieto R, LaJeunesse T. Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc Natl Acad Sci USA. 2015;112:1–8.
LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA. Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) clade D are different species. Phycologia. 2014;53:305–319.
Fricke H, Vareschi E, Schlichter D. Photoecology of the coral Leptoseris fragilis in the Red Sea twilight zone (an experimental study by submersible). Oecologia. 1987;73:371–381.
Gonzalez-Zapata FL, Gómez-Osorio S, Sánchez JA. Conspicuous endolithic algal associations in a mesophotic reef-building coral. Coral Reefs. 2018;37:705–709.
Del Campo J, Pombert JF, Šlapeta J, Larkum A, Keeling PJ. The ‘other’ coral symbiont: Ostreobium diversity and distribution. ISME J. 2017;11:296–299.
Fine M, Loya Y. Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc R Soc B. 2002;269:1205–1210.
Halldal P. Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Biol Bull. 1968;134:411–424.
Fork D, Larkum A. Light harvesting in the green alga Ostreobium sp., a coral symbiont adapted to extreme shade. Mar Biol. 1989;103:381–385.
Hernandez-Agreda A, Gates RD, Ainsworth TD. Defining the core microbiome in corals’ microbial soup. Trends Microbiol. 2017;25:125–140.
Rohwer F, Seguritan V, Azam F, Knowlton N. Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser. 2002;243:1–10.
Williams AD, Brown BE, Putchim L, Sweet MJ. Age-related shifts in bacterial diversity in a reef coral. PLoS ONE. 2015;10:1–16.
Galand PE, Remize M, Meistertzheim AL, Pruski AM, Peru E, Suhrhoff TJ, et al. Diet shapes cold-water corals bacterial communities. Environ Microbiol. 2020;22:354–368.
Schlichter D, Zscharnack B, Krisch H. Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften. 1995;82:561–564.
Lesser MP, Stat M, Gates RD. The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs. 2013;32:603–611.
We sincerely thank the divers of the Under The Pole (UTP) Team: GB, JL, GL who performed the extreme CCR deep dive to 172 m depth to collect the specimens for this study. In addition, we are grateful to all UTP III Expedition crew who greatly contributed to the success of the one-year-long mesophotic expedition. We also thank West N for assistance with the BIO2MAR platform. We acknowledge del Campo J for constructive discussions on Ostreobium phylogeny and sharing his updated 16S-sequences database. We are also grateful for constructive reviews from Hume B and one anonymous referee. This research was funded by the ANR DEEPHOPE (ANRAAPG 2017 #168722), the Délégation à la Recherche DEEPCORAL, the CNRS DEEPREEF and the IFRECOR. MM was supported by NSF OCE 1442206. The technical dives for coral sampling were funded through the Under The Pole Expedition III.
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G. Bardout9, E. Périé-Bardout9, E. Marivint9, G. Lagarrigue9, J. Leblond9, F. Gazzola9, S. Pujolle9, N. Mollon9, A. Mittau9, J. Fauchet9, N. Paulme9, R. Pete9, K. Peyrusse9, A. Ferucci9, A. Magnan9, M. Horlaville9, C. Breton9, M. Gouin9, T. Markocic9, I. Jubert9, P. Herrmann9.
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Rouzé, H., Galand, P.E., Medina, M. et al. Symbiotic associations of the deepest recorded photosynthetic scleractinian coral (172 m depth). ISME J (2021). https://doi.org/10.1038/s41396-020-00857-y