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Annual Review of Genetics

Volume 57, 2023

Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach

Abstract

Symbiotic interactions occur in all domains of life, providing organisms with resources to adapt to new habitats. A prime example is the endosymbiosis between corals and photosynthetic dinoflagellates. Eukaryotic dinoflagellate symbionts reside inside coral cells and transfer essential nutrients to their hosts, driving the productivity of the most biodiverse marine ecosystem. Recent advances in molecular and genomic characterization have revealed symbiosis-specific genes and mechanisms shared among symbiotic cnidarians. In this review, we focus on the cellular and molecular processes that underpin the interaction between symbiont and host. We discuss symbiont acquisition via phagocytosis, modulation of host innate immunity, symbiont integration into host cell metabolism, and nutrient exchange as a fundamental aspect of stable symbiotic associations. We emphasize the importance of using model systems to dissect the cellular complexity of endosymbiosis, which ultimately serves as the basis for understanding its ecology and capacity to adapt in the face of climate change.

Keyword(s): coral reefs, endosymbiosis, innate immunity, model system, nutrient exchange, phagocytosis
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2023-11-27
2024-04-27
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Literature Cited

  1. 1.
    Aihara Y, Maruyama S, Baird AH, Iguchi A, Takahashi S, Minagawa J. 2019. Green fluorescence from cnidarian hosts attracts symbiotic algae. PNAS 116:62118–23
     [Google Scholar]
  2. 2.
    Alvarez M, Casadevall A. 2006. Phagosome extrusion and host-cell survival after Cryptococcus neoformans phagocytosis by macrophages. Curr. Biol. 16:212161–65
     [Google Scholar]
  3. 3.
    Baird AH, Guest JR, Willis BL. 2009. Systematic and biogeographical patterns in the reproductive biology of scleractinian corals. Annu. Rev. Ecol. Evol. Syst. 40:551–71
     [Google Scholar]
  4. 4.
    Baker AC. 2001. Reef corals bleach to survive change. Nature 411:6839765–66
     [Google Scholar]
  5. 5.
    Baker AC. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34:661–89
     [Google Scholar]
  6. 6.
    Barnay-Verdier S, Dall'Osso D, Joli N, Olivré J, Priouzeau F et al. 2013. Establishment of primary cell culture from the temperate symbiotic cnidarian, Anemonia viridis. Cytotechnology 65:5697–704
     [Google Scholar]
  7. 7.
    Barott KL, Thies AB, Tresguerres M. 2022. V-type H+-ATPase in the symbiosome membrane is a conserved mechanism for host control of photosynthesis in anthozoan photosymbioses. R. Soc. Open Sci. 9:1211449
     [Google Scholar]
  8. 8.
    Barott KL, Venn AA, Perez SO, Tambutté S, Tresguerres M. 2015. Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. PNAS 112:2607–12
     [Google Scholar]
  9. 9.
    Barton GM, Kagan JC. 2009. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9:8535–42
     [Google Scholar]
  10. 10.
    Baumgarten S, Simakov O, Esherick LY, Liew YJ, Lehnert EM et al. 2015. The genome of Aiptasia, a sea anemone model for coral symbiosis. PNAS 112:3811893–98
     [Google Scholar]
  11. 11.
    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 273:15992305–12
     [Google Scholar]
  12. 12.
    Berthelier J, Schnitzler CE, Wood-Charlson EM, Poole AZ, Weis VM, Detournay O. 2017. Implication of the host TGFβ pathway in the onset of symbiosis between larvae of the coral Fungia scutaria and the dinoflagellate Symbiodinium sp. (clade C1f). Coral Reefs 36:41263–68
     [Google Scholar]
  13. 13.
    Bhattacharya D, Stephens TG, Tinoco AI, Richmond RH, Cleves PA. 2022. Life on the edge: Hawaiian model for coral evolution. Limnol. Oceanogr. 67:1976–85
     [Google Scholar]
  14. 14.
    Biquand E, Okubo N, Aihara Y, Rolland V, Hayward DC et al. 2017. Acceptable symbiont cell size differs among cnidarian species and may limit symbiont diversity. ISME J. 11:71702–12
     [Google Scholar]
  15. 15.
    Bonacolta AM, Weiler BA, Porta-Fitó T, Sweet M, Keeling P, del Campo J. 2023. Beyond the Symbiodiniaceae: diversity and role of microeukaryotic coral symbionts. Coral Reefs 42:567–77
     [Google Scholar]
  16. 16.
    Boulais J, Trost M, Landry CR, Dieckmann R, Levy ED et al. 2010. Molecular characterization of the evolution of phagosomes. Mol. Syst. Biol. 6:423
     [Google Scholar]
  17. 17.
    Bourne DG, Morrow KM, Webster NS. 2016. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70:317–40
     [Google Scholar]
  18. 18.
    Brucker RM, Bordenstein SR. 2012. Speciation by symbiosis. Trends Ecol. Evol. 27:8443–451
     [Google Scholar]
  19. 19.
    Bucher M, Jones VAS, Hambleton EA, Guse A. 2017. Microinjection to deliver protein and mRNA into zygotes of the cnidarian endosymbiosis model. Sci. Rep. 8:16437
     [Google Scholar]
  20. 20.
    Bucher M, Wolfowicz I, Voss PA, Hambleton EA, Guse A. 2016. Development and symbiosis establishment in the cnidarian endosymbiosis model Aiptasia sp. Sci. Rep. 6:19867
     [Google Scholar]
  21. 21.
    Changsut I, Womack HR, Shickle A, Sharp KH, Fuess LE. 2022. Variation in symbiont density is linked to changes in constitutive immunity in the facultatively symbiotic coral, Astrangia poculata. Biol. Lett. 18:1120220273
     [Google Scholar]
  22. 22.
    Chen M-C, Cheng Y-M, Hong M-C, Fang L-S. 2004. Molecular cloning of Rab5 (ApRab5) in Aiptasia pulchella and its retention in phagosomes harboring live zooxanthellae. Biochem. Biophys. Res. Commun. 324:31024–33
     [Google Scholar]
  23. 23.
    Chen MC, Cheng YM, Sung PJ, Kuo CE, Fang LS. 2003. Molecular identification of Rab7 (ApRab7) in Aiptasia pulchella and its exclusion from phagosomes harboring zooxanthellae. Biochem. Biophys. Res. Commun. 308:3586–95
     [Google Scholar]
  24. 24.
    Cleves PA, Strader ME, Bay LK, Pringle JR, Matz MV 2018. CRISPR/Cas9-mediated genome editing in a reef-building coral. PNAS 115:205235–40
     [Google Scholar]
  25. 25.
    Cleves PA, Tinoco AI, Bradford J, Perrin D, Bay LK, Pringle JR. 2020. Reduced thermal tolerance in a coral carrying CRISPR-induced mutations in the gene for a heat-shock transcription factor. PNAS 117:4628899–905
     [Google Scholar]
  26. 26.
    Coffroth MA, Lewis CF, Santos SR, Weaver JL. 2006. Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr. Biol. 16:23R985–87
     [Google Scholar]
  27. 27.
    Cotinat P, Fricano C, Toullec G, Röttinger E, Barnay-Verdier S, Furla P. 2022. Intrinsically high capacity of animal cells from a symbiotic cnidarian to deal with pro-oxidative conditions. Front. Physiol. 13:819111
     [Google Scholar]
  28. 28.
    Cui G, Liew YJ, Konciute MK, Zhan Y, Hung S-H et al. 2022. Nutritional control regulates symbiont proliferation and life history in coral–dinoflagellate symbiosis. BMC Biol. 20:103
     [Google Scholar]
  29. 29.
    Cumbo VR, Baird AH, van Oppen MJH. 2013. The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32:1111–20
     [Google Scholar]
  30. 30.
    Cziesielski MJ, Liew YJ, Cui G, Aranda M. 2022. Increased incompatibility of heterologous algal symbionts under thermal stress in the cnidarian-dinoflagellate model Aiptasia. Commun. Biol. 5:760
     [Google Scholar]
  31. 31.
    Dani V, Priouzeau F, Mertz M, Mondin M, Pagnotta S et al. 2017. Expression patterns of sterol transporters NPC1 and NPC2 in the cnidarian–dinoflagellate symbiosis. Cell Microbiol. 19:10e12753
     [Google Scholar]
  32. 32.
    Davies SW, Marchetti A, Ries JB, Castillo KD. 2016. Thermal and pCO2 stress elicit divergent transcriptomic responses in a resilient coral. Front. Mar. Sci. 3:112
     [Google Scholar]
  33. 33.
    Davies SW, Strader ME, Kool JT, Kenkel CD, Matz MV. 2017. Modeled differences of coral life-history traits influence the refugium potential of a remote Caribbean reef. Coral Reefs 36:3913–25
     [Google Scholar]
  34. 34.
    Davy SK, Allemand D, Weis VM. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:2229–61
     [Google Scholar]
  35. 35.
    Davy SK, Lucas IAN, Turner JR. 1997. Uptake and persistence of homologous and heterologous zooxanthellae in the temperate sea anemone Cereus pedunculatus (Pennant). Biol. Bull. 192:2208–16
     [Google Scholar]
  36. 36.
    de Vries J, Archibald JM. 2017. Endosymbiosis: Did plastids evolve from a freshwater cyanobacterium?. Curr. Biol. 27:3R103–5
     [Google Scholar]
  37. 37.
    Desalvo MK, Sunagawa S, Voolstra CR, Medina M. 2010. Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar. Ecol. Prog. Ser. 402:97–113
     [Google Scholar]
  38. 38.
    Domart-Coulon IJ, Elbert DC, Scully EP, Calimlim PS, Ostrander GK. 2001. Aragonite crystallization in primary cell cultures of multicellular isolates from a hard coral, Pocillopora damicornis. PNAS 98:2111885–90
     [Google Scholar]
  39. 39.
    Dunkelberger JR, Song W-C. 2010. Complement and its role in innate and adaptive immune responses. Cell Res. 20:34–50
     [Google Scholar]
  40. 40.
    Dunn SR, Weis VM. 2009. Apoptosis as a post-phagocytic winnowing mechanism in a coral–dinoflagellate mutualism. Environ. Microbiol. 11:1268–76
     [Google Scholar]
  41. 41.
    Dupuy AG, Caron E. 2008. Integrin-dependent phagocytosis—spreading from microadhesion to new concepts. J. Cell Sci. 121:111773–83
     [Google Scholar]
  42. 42.
    Ferrier-Pagès C, Leal MC. 2019. Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses. Ecol. Evol. 9:1723–40
     [Google Scholar]
  43. 43.
    Flannagan RS, Cosío G, Grinstein S. 2009. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7:355–66
     [Google Scholar]
  44. 44.
    Franzenburg S, Fraune S, Künzel S, Baines JF, Domazet-Lošo T, Bosch TCG. 2012. MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers. PNAS 109:4719374–79
     [Google Scholar]
  45. 45.
    Ganot P, Moya A, Magnone V, Allemand D, Furla P, Sabourault C. 2011. Adaptations to endosymbiosis in a cnidarian-dinoflagellate association: differential gene expression and specific gene duplications. PLOS Genet. 7:7e1002187
     [Google Scholar]
  46. 46.
    González-Pech RA, Ragan MA, Chan CX. 2017. Signatures of adaptation and symbiosis in genomes and transcriptomes of Symbiodinium. Sci. Rep. 7:15021
     [Google Scholar]
  47. 47.
    Gorman LM, Konciute MK, Cui G, Oakley CA, Grossman AR et al. 2022. Symbiosis with dinoflagellates alters cnidarian cell-cycle gene expression. Cell Microbiol. 2022:3330160
     [Google Scholar]
  48. 48.
    Gornik SG, Maegele I, Hambleton EA, Voss PA, Waller RF, Guse A. 2022. Nuclear transformation of a dinoflagellate symbiont of corals. Front. Mar. Sci. 9:1035413
     [Google Scholar]
  49. 49.
    Grawunder D, Hambleton EA, Bucher M, Wolfowicz I, Bechtoldt N, Guse A. 2015. Induction of gametogenesis in the cnidarian endosymbiosis model Aiptasia sp. Sci. Rep. 5:15677
     [Google Scholar]
  50. 50.
    Hamada M, Shoguchi E, Shinzato C, Kawashima T, Miller DJ, Satoh N. 2013. The complex NOD-like receptor repertoire of the coral Acropora digitifera includes novel domain combinations. Mol. Biol. Evol. 30:1167–76
     [Google Scholar]
  51. 51.
    Hambleton EA, Guse A, Pringle JR. 2014. Similar specificities of symbiont uptake by adults and larvae in an anemone model system for coral biology. J. Exp. Biol. 217:91613–19
     [Google Scholar]
  52. 52.
    Hambleton EA, Jones VAS, Maegele I, Kvaskoff D, Sachsenheimer T, Guse A. 2019. Sterol transfer by atypical cholesterol-binding NPC2 proteins in coral-algal symbiosis. eLife 8:e43923
     [Google Scholar]
  53. 53.
    Herrera M, Klein SG, Campana S, Chen JE, Prasanna A et al. 2021. Temperature transcends partner specificity in the symbiosis establishment of a cnidarian. ISME J. 15:1141–53
     [Google Scholar]
  54. 54.
    Hoadley KD, Lewis AM, Wham DC, Pettay DT, Grasso C et al. 2019. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci. Rep. 9:9985
     [Google Scholar]
  55. 55.
    Hollingsworth LL, Kinzie RA, Lewis TD, Krupp DA, Leong JAC. 2005. Phototaxis of motile zooxanthellae to green light may facilitate symbiont capture by coral larvae. Coral Reefs 24:4523
     [Google Scholar]
  56. 56.
    Houlbrèque F, Ferrier-Pagès C. 2009. Heterotrophy in tropical scleractinian corals. Biol. Rev. 84:11–17
     [Google Scholar]
  57. 57.
    Hu M, Zheng X, Fan CM, Zheng Y. 2020. Lineage dynamics of the endosymbiotic cell type in the soft coral Xenia. Nature 582:7813534–38
     [Google Scholar]
  58. 58.
    Ishii Y, Maruyama S, Fujimura-Kamada K, Kutsuna N, Takahashi S et al. 2018. Isolation of uracil auxotroph mutants of coral symbiont alga for symbiosis studies. Sci. Rep. 8:3237
     [Google Scholar]
  59. 59.
    Ishii Y, Maruyama S, Takahashi H, Aihara Y, Yamaguchi T et al. 2019. Global shifts in gene expression profiles accompanied with environmental changes in cnidarian-dinoflagellate endosymbiosis. G3 9:72337–47
     [Google Scholar]
  60. 60.
    Jacobovitz MR, Rupp S, Voss PA, Maegele I, Gornik SG, Guse A. 2021. Dinoflagellate symbionts escape vomocytosis by host cell immune suppression. Nat. Microbiol. 6:6769–82
     [Google Scholar]
  61. 61.
    Jaumouillé V, Grinstein S. 2016. Molecular mechanisms of phagosome formation. Microbiol. Spectr. 4:3 https://doi.org/10.1128/microbiolspec.mchd-0013-2015
    [Google Scholar]
  62. 62.
    Jinkerson RE, Russo JA, Newkirk CR, Kirk AL, Chi RJ et al. 2022. Cnidarian-Symbiodiniaceae symbiosis establishment is independent of photosynthesis. Curr. Biol. 32:112402–15.e4
     [Google Scholar]
  63. 63.
    Jones VAS, Bucher M, Hambleton EA, Guse A. 2018. Microinjection to deliver protein, mRNA, and DNA into zygotes of the cnidarian endosymbiosis model Aiptasia sp. Sci. Rep. 8:16437
     [Google Scholar]
  64. 64.
    Kawai T, Akira S. 2007. Signaling to NF-κB by Toll-like receptors. Trends Mol. Med. 13:11460–69
     [Google Scholar]
  65. 65.
    Kawamura K, Nishitsuji K, Shoguchi E, Fujiwara S, Satoh N. 2021. Establishing sustainable cell lines of a coral, Acropora tenuis. Mar. Biotechnol. 23:3373–88
     [Google Scholar]
  66. 66.
    Kayal E, Bentlage B, Sabrina Pankey M, Ohdera AH, Medina M et al. 2018. Phylogenomics provides a robust topology of the major cnidarian lineages and insights on the origins of key organismal traits. BMC Evol. Biol. 18:68
     [Google Scholar]
  67. 67.
    Kayal E, Roure B, Philippe H, Collins AG, Lavrov DV. 2013. Cnidarian phylogenetic relationships as revealed by mitogenomics. BMC Evol. Biol. 13:5
     [Google Scholar]
  68. 68.
    Kopp C, Wisztorski M, Revel J, Mehiri M, Dani V et al. 2015. MALDI-MS and NanoSIMS imaging techniques to study cnidarian–dinoflagellate symbioses. Zoology 118:2125–31
     [Google Scholar]
  69. 69.
    Krueger T, Bodin J, Horwitz N, Loussert-Fonta C, Sakr A et al. 2018. Temperature and feeding induce tissue level changes in autotrophic and heterotrophic nutrient allocation in the coral symbiosis—a NanoSIMS study. Sci. Rep. 8:12710
     [Google Scholar]
  70. 70.
    Kvennefors ECE, Leggat W, Kerr CC, Ainsworth TD, Hoegh-Guldberg O, Barnes AC. 2010. Analysis of evolutionarily conserved innate immune components in coral links immunity and symbiosis. Dev. Comp. Immunol. 34:111219–29
     [Google Scholar]
  71. 71.
    Kwong WK, del Campo J, Mathur V, Vermeij MJA, Keeling PJ. 2019. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568:7750103–7
     [Google Scholar]
  72. 72.
    LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T et al. 2004. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar. Ecol. Prog. Ser. 284:147–61
     [Google Scholar]
  73. 73.
    LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD et al. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28:162570–80.e6
     [Google Scholar]
  74. 74.
    LaJeunesse TC, Wiedenmann J, Casado-Amezúa P, D'Ambra I, Turnham KE et al. 2022. Revival of Philozoon Geddes for host-specialized dinoflagellates, ‘zooxanthellae’, in animals from coastal temperate zones of northern and southern hemispheres. Eur. J. Phycol. 57:2166–80
     [Google Scholar]
  75. 75.
    Lehnert EM, Mouchka ME, Burriesci MS, Gallo ND, Schwarz JA, Pringle JR. 2014. Extensive differences in gene expression between symbiotic and aposymbiotic cnidarians. G3 4:2277–95
     [Google Scholar]
  76. 76.
    Lesser MP, Stat M, Gates RD. 2013. The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32:3603–11
     [Google Scholar]
  77. 77.
    Levy S, Elek A, Grau-Bové X, Menéndez-Bravo S, Iglesias M et al. 2021. A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity. Cell 184:112973–87.e18
     [Google Scholar]
  78. 78.
    Lewis CL, Coffroth MA. 2004. The acquisition of exogenous, algal symbionts by an octocoral after bleaching. Science 304:56761490–92
     [Google Scholar]
  79. 79.
    Lin KL, Wang JT, Fang LS. 2000. Participation of glycoproteins on zooxanthellal cell walls in the establishment of a symbiotic relationship with the sea anemone, Aiptasia pulchella. Zool. Stud. 39:3172–78
     [Google Scholar]
  80. 80.
    Logan DDK, LaFlamme AC, Weis VM, Davy SK. 2010. Flow-cytometric characterization of the cell-surface glycans of symbiotic dinoflagellates (Symbiodinium spp.). J. Phycol. 46:3525–33
     [Google Scholar]
  81. 81.
    Loussert-Fonta C, Toullec G, Paraecattil AA, Jeangros Q, Krueger T et al. 2020. Correlation of fluorescence microscopy, electron microscopy, and NanoSIMS stable isotope imaging on a single tissue section. Commun. Biol. 3:362
     [Google Scholar]
  82. 82.
    Ma H, Croudace JE, Lammas DA, May RC 2006. Expulsion of live pathogenic yeast by macrophages. Curr. Biol. 16:212156–60
     [Google Scholar]
  83. 83.
    Maegele I, Rupp S, Özbek S, Guse A, Hambleton EA, Holstein TW. 2023. A predatory gastrula leads to symbiosis-independent settlement in Aiptasia. PNAS 12040e2311872120
  84. 84.
    Mandel MJ. 2010. Models and approaches to dissect host-symbiont specificity. Trends Microbiol. 18:11504–11
     [Google Scholar]
  85. 85.
    Manifava M, Smith M, Rotondo S, Walker S, Niewczas I et al. 2016. Dynamics of mTORC1 activation in response to amino acids. eLife 5:e19960
     [Google Scholar]
  86. 86.
    Mansfield KM, Carter NM, Nguyen L, Cleves PA, Alshanbayeva A et al. 2017. Transcription factor NF-κB is modulated by symbiotic status in a sea anemone model for cnidarian bleaching. Sci. Rep. 7:16025
     [Google Scholar]
  87. 87.
    Mansour TA, Rosenthal JJC, Brown CT, Roberson LM. 2016. Transcriptome of the Caribbean stony coral Porites astreoides from three developmental stages. Gigascience 5:133
     [Google Scholar]
  88. 88.
    Maor-Landaw K, Eisenhut M, Tortorelli G, van de Meene A, Kurz S et al. 2023. A candidate transporter allowing symbiotic dinoflagellates to feed their coral hosts. ISME Commun. 3:7
     [Google Scholar]
  89. 89.
    Maor-Landaw K, van Oppen MJH, McFadden GI. 2019. Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae). Ecol. Evol. 10:1451–66
     [Google Scholar]
  90. 90.
    Marinov GK, Trevino AE, Xiang T, Kundaje A, Grossman AR, Greenleaf WJ. 2021. Transcription-dependent domain-scale three-dimensional genome organization in the dinoflagellate Breviolum minutum. Nat. Genet. 53:5613–17
     [Google Scholar]
  91. 91.
    Martin WF, Garg S, Zimorski V. 2015. Endosymbiotic theories for eukaryote origin. Philos. Trans. R. Soc. B 370:167820140330
     [Google Scholar]
  92. 92.
    Maruyama S, Mandelare-Ruiz PE, McCauley M, Peng W, Cho BG et al. 2022. Heat stress of algal partner hinders colonization success and alters the algal cell surface glycome in a cnidarian-algal symbiosis. Microbiol. Spectr. 10:3e0156722
     [Google Scholar]
  93. 93.
    Mashini AG, Oakley CA, Beepat SS, Peng L, Grossman AR et al. 2023. The influence of symbiosis on the proteome of the Exaiptasia endosymbiont Breviolum minutum. Microorganisms 11:2292
     [Google Scholar]
  94. 94.
    Mass T, Drake JL, Haramaty L, Rosenthal Y, Schofield OME et al. 2012. Aragonite precipitation by “proto-polyps” in coral cell cultures. PLOS ONE 7:4e35049
     [Google Scholar]
  95. 95.
    Massagué J. 2012. TGFβ signalling in context. Nat. Rev. Mol. Cell Biol. 13:10616–30
     [Google Scholar]
  96. 96.
    Matthews JL, Crowder CM, Oakley CA, Lutz A, Roessner U et al. 2017. Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. PNAS 114:5013194–99
     [Google Scholar]
  97. 97.
    Matthews JL, Oakley CA, Lutz A, Hillyer KE, Roessner U et al. 2018. Partner switching and metabolic flux in a model cnidarian–dinoflagellate symbiosis. Proc. R. Soc. B 285:189220182336
     [Google Scholar]
  98. 98.
    Matthews JL, Sproles AE, Oakley CA, Grossman AR, Weis VM, Davy SK. 2016. Menthol-induced bleaching rapidly and effectively provides experimental aposymbiotic sea anemones (Aiptasia sp.) for symbiosis investigations. J. Exp. Biol. 219:3306–10
     [Google Scholar]
  99. 99.
    McIlroy SE, terHorst CP, Teece M, Coffroth MA. 2022. Nutrient dynamics in coral symbiosis depend on both the relative and absolute abundance of Symbiodiniaceae species. Microbiome 10:192
     [Google Scholar]
  100. 100.
    Medina M, Sharp V, Ohdera A, Bellantuono A, Dalrymple J et al. 2021. The upside-down jellyfish Cassiopea xamachana as an emerging model system to study cnidarian–algal symbiosis. Handbook of Marine Model Organisms in Experimental Biology: Established and Emerging A Boutet, B Schierwater 149–71. Boca Raton, FL: CRC
     [Google Scholar]
  101. 101.
    Medrano E, Merselis DG, Bellantuono AJ, Rodriguez-Lanetty M. 2019. Proteomic basis of symbiosis: A heterologous partner fails to duplicate homologous colonization in a novel cnidarian-Symbiodiniaceae mutualism. Front. Microbiol. 10:1153
     [Google Scholar]
  102. 102.
    Mohamed AR, Cumbo V, Harii S, Shinzato C, Chan CX et al. 2016. The transcriptomic response of the coral Acropora digitifera to a competent Symbiodinium strain: the symbiosome as an arrested early phagosome. Mol. Ecol. 25:133127–41
     [Google Scholar]
  103. 103.
    Moran NA. 2006. Symbiosis. Curr. Biol. 16:20R866–71
     [Google Scholar]
  104. 104.
    Morris LA, Voolstra CR, Quigley KM, Bourne DG, Bay LK. 2019. Nutrient availability and metabolism affect the stability of coral–Symbiodiniaceae symbioses. Trends Microbiol. 27:8678–89
     [Google Scholar]
  105. 105.
    Muscatine L. 1990. The role of symbiotic algae in carbon and energy flux in reef corals. Ecosyst. World 25:75–87
     [Google Scholar]
  106. 106.
    Muscatine L, Goiran C, Land L, Jaubert J, Cuif JP, Allemand D. 2005. Stable isotopes (δ13C and δ15N) of organic matrix from coral skeleton. PNAS 102:51525–30
     [Google Scholar]
  107. 107.
    Nawaz K, Cziesielski MJ, Mariappan KG, Cui G, Aranda M. 2022. Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia. BMC Biol. 20:265
     [Google Scholar]
  108. 108.
    Ndungu FM, Urban BC, Marsh K, Langhorne J. 2005. Regulation of immune response by Plasmodium-infected red blood cells. Parasite Immunol. 27:10/11373–84
     [Google Scholar]
  109. 109.
    Neubauer E-F, Poole AZ, Neubauer P, Detournay O, Tan K et al. 2017. A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian-dinoflagellate symbiosis. eLife 6:e24494
     [Google Scholar]
  110. 110.
    Nyholm SV, McFall-Ngai MJ. 2004. The winnowing: establishing the squid–Vibrio symbiosis. Nat. Rev. Microbiol. 2:8632–42
     [Google Scholar]
  111. 111.
    Oakley CA, Ameismeier MF, Peng L, Weis VM, Grossman AR, Davy SK. 2016. Symbiosis induces widespread changes in the proteome of the model cnidarian Aiptasia. Cell Microbiol. 18:71009–23
     [Google Scholar]
  112. 112.
    Oakley CA, Davy SK 2018. Cell biology of coral bleaching. Coral Bleaching M van Oppen, J Lough 189–211. Cham, Switz.: Springer
     [Google Scholar]
  113. 113.
    Parkinson JE, Tivey TR, Mandelare PE, Adpressa DA, Loesgen S, Weis VM. 2018. Subtle differences in symbiont cell surface glycan profiles do not explain species-specific colonization rates in a model cnidarian-algal symbiosis. Front. Microbiol. 9:842
     [Google Scholar]
  114. 114.
    Peng SE, Chen W-NU, Chen H-K, Lu C-Y, Mayfield AB et al. 2011. Lipid bodies in coral-dinoflagellate endosymbiosis: proteomic and ultrastructural studies. Proteomics 11:173540–55
     [Google Scholar]
  115. 115.
    Pernice M, Meibom A, Van Den Heuvel A, Kopp C, Domart-Coulon I et al. 2012. A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis. ISME J. 6:71314–24
     [Google Scholar]
  116. 116.
    Pinzón JH, Kamel B, Burge CA, Harvell CD, Medina M et al. 2015. Whole transcriptome analysis reveals changes in expression of immune-related genes during and after bleaching in a reef-building coral. R. Soc. Open Sci. 2:4140214
     [Google Scholar]
  117. 117.
    Poole AZ, Kitchen SA, Weis VM. 2016. The role of complement in cnidarian-dinoflagellate symbiosis and immune challenge in the sea anemone Aiptasia pallida. Front. Microbiol. 7:519
     [Google Scholar]
  118. 118.
    Puntin G, Craggs J, Hayden R, Engelhardt KE, McIlroy S et al. 2022. The reef-building coral Galaxea fascicularis: a new model system for coral symbiosis research. Coral Reefs 42:239–52
     [Google Scholar]
  119. 119.
    Putnam HM, Barott KL, Ainsworth TD, Gates RD. 2017. The vulnerability and resilience of reef-building corals. Curr. Biol. 27:11R528–40
     [Google Scholar]
  120. 120.
    Quigley KM, Willis BL, Kenkel CD. 2019. Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata. Sci. Rep. 9:13328
     [Google Scholar]
  121. 121.
    Rädecker N, Pogoreutz C, Gegner HM, Cárdenas A, Roth F et al. 2021. Heat stress destabilizes symbiotic nutrient cycling in corals. PNAS 118:5e2022653118
     [Google Scholar]
  122. 122.
    Rädecker N, Raina JB, Pernice M, Perna G, Guagliardo P et al. 2018. Using Aiptasia as a model to study metabolic interactions in cnidarian-Symbiodinium symbioses. Front. Physiol. 9:214
     [Google Scholar]
  123. 123.
    Reaka-Kudla ML. 1997. The global biodiversity of coral reefs: a comparison with rain forests. Biodiversity II: Understanding and Protecting Our Biological Resources ML Reaka-Kudla, DE Wilson, EO Wilson 83–108. Washington, DC: Joseph Henry
     [Google Scholar]
  124. 124.
    Reich HG, Robertson DL, Goodbody-Gringley G. 2017. Do the shuffle: changes in Symbiodinium consortia throughout juvenile coral development. PLOS ONE 12:2e0171768
     [Google Scholar]
  125. 125.
    Revel J, Massi L, Mehiri M, Boutoute M, Mayzaud P et al. 2016. Differential distribution of lipids in epidermis, gastrodermis and hosted Symbiodinium in the sea anemone Anemonia viridis. Comp. Biochem. Physiol. A 191:140–51
     [Google Scholar]
  126. 126.
    Rivera HE, Davies SW. 2021. Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity. Sci. Rep. 11:21226
     [Google Scholar]
  127. 127.
    Rodriguez-Lanetty M, Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM. 2006. Temporal and spatial infection dynamics indicate recognition events in the early hours of a dinoflagellate/coral symbiosis. Mar. Biol. 149:4713–19
     [Google Scholar]
  128. 128.
    Roger LM, Reich HG, Lawrence E, Li S, Vizgaudis W et al. 2021. Applying model approaches in non-model systems: a review and case study on coral cell culture. PLOS ONE 16:4e0248953
     [Google Scholar]
  129. 129.
    Ros M, Suggett DJ, Edmondson J, Haydon T, Hughes DJ et al. 2021. Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta. Coral Reefs 40:2595–607
     [Google Scholar]
  130. 130.
    Rosales C, Uribe-Querol E. 2017. Phagocytosis: a fundamental process in immunity. Biomed. Res. Int. 2017:9042851
     [Google Scholar]
  131. 131.
    Rosenstiel P, Philipp EER, Schreiber S, Bosch TCG. 2009. Evolution and function of innate immune receptors—insights from marine invertebrates. J. Innate Immun. 1:4291–300
     [Google Scholar]
  132. 132.
    Rosset SL, Oakley CA, Ferrier-Pagès C, Suggett DJ, Weis VM, Davy SK. 2021. The molecular language of the cnidarian–dinoflagellate symbiosis. Trends Microbiol. 29:4320–33
     [Google Scholar]
  133. 133.
    Rosset SL, Wiedenmann J, Reed AJ, D'Angelo C 2017. Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates. Mar. Pollut. Bull. 118:1/2180–87
     [Google Scholar]
  134. 134.
    Roth E, Jeon K, Stacey G 1988. Homology in endosymbiotic systems: the term ‘symbiosome. .’ In Molecular Genetics of Plant-Microbe Interactions R Palacios, DPS Verma 220–25. St. Paul, MN: Am. Phytopathol. Soc.
     [Google Scholar]
  135. 135.
    Rubin ET, Enochs IC, Foord C, Mayfield AB, Kolodziej G et al. 2021. Molecular mechanisms of coral persistence within highly urbanized locations in the Port of Miami, Florida. Front. Mar. Sci. 8:695236
     [Google Scholar]
  136. 136.
    Savini M, Zhao Q, Wang MC. 2019. Lysosomes: signaling hubs for metabolic sensing and longevity. Trends Cell Biol. 29:11876–87
     [Google Scholar]
  137. 137.
    Schwarz JA. 2008. Understanding the intracellular niche in cnidarian-Symbiodinium symbioses: Parasites lead the way. Vie Milieu 58:2141–51
     [Google Scholar]
  138. 138.
    Seoane PI, May RC 2020. Vomocytosis: what we know so far. Cell Microbiol. 22:2e13145
     [Google Scholar]
  139. 139.
    Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K et al. 2011. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:7360320–23
     [Google Scholar]
  140. 140.
    Souter D, Planes S, Wicquart J, Logan M, Obura D, Staub F. 2020. Status of coral reefs of the world: 2020 Rep. Glob. Coral Reef Monit. Netw. Canberra, Aust:.
  141. 141.
    Spalding MD, Grenfell AM. 1997. New estimates of global and regional coral reef areas. Coral Reefs 16:4225–30
     [Google Scholar]
  142. 142.
    Sproles AE, Oakley CA, Krueger T, Grossman AR, Weis VM et al. 2020. Sub-cellular imaging shows reduced photosynthetic carbon and increased nitrogen assimilation by the non-native endosymbiont Durusdinium trenchii in the model cnidarian Aiptasia. Environ. Microbiol. 22:93741–53
     [Google Scholar]
  143. 143.
    Sproles AE, Oakley CA, Matthews JL, Peng L, Owen JG et al. 2019. Proteomics quantifies protein expression changes in a model cnidarian colonised by a thermally tolerant but suboptimal symbiont. ISME J. 13:92334–45
     [Google Scholar]
  144. 144.
    Takeuchi R, Jimbo M, Tanimoto F, Iijima M, Yamashita H, Suzuki G. 2021. N-Acetyl-d-glucosamine-binding lectin in Acropora tenuis attracts specific Symbiodiniaceae cell culture strains. Mar. Drugs 19:3146
     [Google Scholar]
  145. 145.
    Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW. 2006. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148:4711–22
     [Google Scholar]
  146. 146.
    Tivey TR, Parkinson JE, Mandelare PE, Adpressa DA, Peng W et al. 2020. N-linked surface glycan biosynthesis, composition, inhibition, and function in cnidarian-dinoflagellate symbiosis. Microb. Ecol. 80:1223–36
     [Google Scholar]
  147. 147.
    Tivey TR, Parkinson JE, Weis VM. 2020. Host and symbiont cell cycle coordination is mediated by symbiotic state, nutrition, and partner identity in a model cnidarian-dinoflagellate symbiosis. mBio 11:202626
     [Google Scholar]
  148. 148.
    Tolleter D, Seneca FO, Denofrio JC, Krediet CJ, Palumbi SR et al. 2013. Coral bleaching independent of photosynthetic activity. Curr. Biol. 23:181782–86
     [Google Scholar]
  149. 149.
    Tortorelli G, Oakley CA, Davy SK, van Oppen MJH, McFadden GI. 2022. Cell wall proteomic analysis of the cnidarian photosymbionts Breviolum minutum and Cladocopium goreaui. J. Eukaryot. Microbiol. 69:1e12870
     [Google Scholar]
  150. 150.
    Tortorelli G, Rautengarten C, Bacic A, Segal G, Ebert B et al. 2022. Cell surface carbohydrates of symbiotic dinoflagellates and their role in the establishment of cnidarian-dinoflagellate symbiosis. ISME J. 16:1190–99
     [Google Scholar]
  151. 151.
    Traylor-Knowles N, Rose NH, Sheets EA, Palumbi SR. 2017. Early transcriptional responses during heat stress in the coral Acropora hyacinthus. Biol. Bull. 232:291–100
     [Google Scholar]
  152. 152.
    Tsang Min Ching SJ, Chan WY, Perez-Gonzalez A, Hillyer KE, Buerger P, van Oppen MJH. 2022. Colonization and metabolite profiles of homologous, heterologous and experimentally evolved algal symbionts in the sea anemone Exaiptasia diaphana. ISME Commun. 2:130
     [Google Scholar]
  153. 153.
    Uribe-Querol E, Rosales C. 2020. Phagocytosis: our current understanding of a universal biological process. Front. Immunol. 11:1066
     [Google Scholar]
  154. 154.
    Ventura P, Toullec G, Fricano C, Chapron L, Meunier V et al. 2018. Cnidarian primary cell culture as a tool to investigate the effect of thermal stress at cellular level. Mar. Biotechnol. 20:2144–54
     [Google Scholar]
  155. 155.
    Voolstra CR. 2013. A journey into the wild of the cnidarian model system Aiptasia and its symbionts. Mol. Ecol. 22:174366–68
     [Google Scholar]
  156. 156.
    Voolstra CR, Schwarz JA, Schnetzer J, Sunagawa S, Desalvo MK et al. 2009. The host transcriptome remains unaltered during the establishment of coral-algal symbioses. Mol. Ecol. 18:91823–33
     [Google Scholar]
  157. 157.
    Voss PA, Gornik SG, Jacobovitz MR, Rupp S, Dörr MS et al. 2023. Host nutrient sensing is mediated by mTOR signaling in cnidarian-dinoflagellate symbiosis. Curr. Biol. 33173634–47.E5
  158. 158.
    Wahl SM. 1994. Transforming growth factor β: the good, the bad, and the ugly. J. Exp. Med. 180:51589–90
     [Google Scholar]
  159. 159.
    Wakefield TS, Kempf SC. 2001. Development of host- and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biol. Bull. 200:2127–43
     [Google Scholar]
  160. 160.
    Wang C, Arneson EM, Gleason DF, Hopkinson BM. 2021. Resilience of the temperate coral Oculina arbuscula to ocean acidification extends to the physiological level. Coral Reefs 40:1201–14
     [Google Scholar]
  161. 161.
    Wartosch L, Bright NA, Luzio JP. 2015. Lysosomes. Curr. Biol. 25:28R315–16
     [Google Scholar]
  162. 162.
    Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR. 2008. Cell biology in model systems as the key to understanding corals. Trends Ecol. Evol. 23:7369–76
     [Google Scholar]
  163. 163.
    Weis VM, Reynolds WS, DeBoer MD, Krupp DA. 2001. Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbiodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:3301–8
     [Google Scholar]
  164. 164.
    Wiedenmann J, D'Angelo C, Smith EG, Hunt AN, Legiret FE et al. 2013. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3:2160–64
     [Google Scholar]
  165. 165.
    Williams LM, Fuess LE, Brennan JJ, Mansfield KM, Salas-Rodriguez E et al. 2018. A conserved Toll-like receptor-to-NF-κB signaling pathway in the endangered coral Orbicella faveolata. Dev. Comp. Immunol. 79:128–36
     [Google Scholar]
  166. 166.
    Wolfowicz I, Baumgarten S, Voss PA, Hambleton EA, Voolstra CR et al. 2016. Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians. Sci. Rep. 6:32366
     [Google Scholar]
  167. 167.
    Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM. 2006. Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol. 8:121985–93
     [Google Scholar]
  168. 168.
    Xiang T, Jinkerson RE, Clowez S, Tran C, Krediet CJ. 2017. Glucose-induced trophic shift in Symbiodinium and its physiological and molecular consequences. Plant Physiol. 176:1793–807
     [Google Scholar]
  169. 169.
    Xiang T, Lehnert E, Jinkerson RE, Clowez S, Kim RG et al. 2020. Symbiont population control by host-symbiont metabolic interaction in Symbiodiniaceae-cnidarian associations. Nat. Commun. 11:108
     [Google Scholar]
  170. 170.
    Yellowlees D, Rees TAV, Leggat W. 2008. Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31:5679–94
     [Google Scholar]
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Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach
Annual Review of Genetics 57, 411 (2023); https://doi.org/10.1146/annurev-genet-072320-125436
/content/journals/10.1146/annurev-genet-072320-125436
/content/journals/10.1146/annurev-genet-072320-125436
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