1932

Abstract

Coral reefs are home to over two million species and provide habitat for roughly 25% of all marine animals, but they are being severely threatened by pollution and climate change. A large amount of genomic, transcriptomic, and other omics data is becoming increasingly available from different species of reef-building corals, the unicellular dinoflagellates, and the coral microbiome (bacteria, archaea, viruses, fungi, etc.). Such new data present an opportunity for bioinformatics researchers and computational biologists to contribute to a timely, compelling, and urgent investigation of critical factors that influence reef health and resilience.

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2022-08-10
2024-06-21
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Literature Cited

  1. 1.
    Hoegh-Guldberg O, Poloczanska ES, Skirving W, Dove S. 2017. Coral reef ecosystems under climate change and ocean acidification. Front. Mar. Sci. 4:158
    [Google Scholar]
  2. 2.
    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. 28:2570–80
    [Google Scholar]
  3. 3.
    Venn A, Loram J, Douglas A. 2008. Photosynthetic symbioses in animals. J. Exp. Bot. 59:1069–80
    [Google Scholar]
  4. 4.
    Hernandez-Agreda A, Leggat W, Bongaerts P, Herrera C, Ainsworth TD. 2018. Rethinking the coral microbiome: simplicity exists within a diverse microbial biosphere. mBio 9:e00812–18
    [Google Scholar]
  5. 5.
    van Oppen MJ, Blackall LL. 2019. Coral microbiome dynamics, functions and design in a changing world. Nat. Rev. Microbiol. 17:557–67
    [Google Scholar]
  6. 6.
    Rohwer F, Seguritan V, Azam F, Knowlton N. 2002. Diversity and distribution of coral-associated bacteria. Mar. Ecol. Prog. Ser. 243:1–10
    [Google Scholar]
  7. 7.
    Bosch TC, McFall-Ngai MJ. 2011. Metaorganisms as the new frontier. Zoology 114:185–90
    [Google Scholar]
  8. 8.
    Putnam HM, Barott KL, Ainsworth TD, Gates RD. 2017. The vulnerability and resilience of reef-building corals. Curr. Biol. 27:R528–40
    [Google Scholar]
  9. 9.
    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. 80:435–71
    [Google Scholar]
  10. 10.
    Nolan MK, Schmidt-Roach S, Davis AR, Aranda M, Howells EJ. 2021. Widespread bleaching in the One Tree Island lagoon (Southern Great Barrier Reef) during record-breaking temperatures in 2020. Environ. Monitor. Assess. 193:590
    [Google Scholar]
  11. 11.
    Oliver EC, Donat MG, Burrows MT, Moore PJ, Smale DA et al. 2018. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9:1324
    [Google Scholar]
  12. 12.
    Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT et al. 2018. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
    [Google Scholar]
  13. 13.
    Voolstra CR, Miller DJ, Ragan MA, Hoffmann A, Hoegh-Guldberg O et al. 2015. The ReFuGe 2020 Consortium—using “omics” approaches to explore the adaptability and resilience of coral holobionts to environmental change. Front. Mar. Sci. 2:68
    [Google Scholar]
  14. 14.
    Comm. Interv. Increase Resil. Coral Reefs, Ocean Studies Board, Board Life Sci 2019. A Research Review of Interventions to Increase the Persistence and Resilience of Coral Reefs Washington, DC: Natl. Acad. Press
    [Google Scholar]
  15. 15.
    Bhattacharya D, Agrawal S, Aranda M, Baumgarten S, Belcaid M et al. 2016. Comparative genomics explains the evolutionary success of reef-forming corals. eLife 5:e13288
    [Google Scholar]
  16. 16.
    Kumar L, Brenner N, Sledieski S, Olaosebikan M, Lynn-Goin M et al. 2022. Transfer of knowledge from model organisms to evolutionarily distant non-model organisms: The coral Pocillopora damicornis membrane signaling receptome. bioRxiv 10.1101/2021.10.18.464760. https://doi.org/10.1101/2021.10.18.464760
    [Crossref]
  17. 17.
    Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S et al. 2013. Draft assembly of the Symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr. Biol. 23:1399–408
    [Google Scholar]
  18. 18.
    Shinzato C, Khalturin K, Inoue J, Zayasu Y, Kanda M et al. 2021. Eighteen coral genomes reveal the evolutionary origin of Acropora strategies to accommodate environmental changes. Mol. Biol. Evol. 38:16–30
    [Google Scholar]
  19. 19.
    Robbins SJ, Singleton CM, Chan CX, Messer LF, Geers AU et al. 2019. A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat. Microbiol. 4:2090–100
    [Google Scholar]
  20. 20.
    Fuller ZL, Mocellin VJ, Morris LA, Cantin N, Shepherd J et al. 2020. Population genetics of the coral Acropora millepora: toward genomic prediction of bleaching. Science 369:6501eaba4674
    [Google Scholar]
  21. 21.
    Williams A, Chiles EN, Conetta D, Pathmanathan JS, Cleves PA et al. 2021. Metabolomic shifts associated with heat stress in coral holobionts. Sci. Adv. 7:eabd4210
    [Google Scholar]
  22. 22.
    Hu M, Zheng X, Fan CM, Zheng Y. 2020. Lineage dynamics of the endosymbiotic cell type in the soft coral Xenia. Nature 582:534–38
    [Google Scholar]
  23. 23.
    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]
  24. 24.
    Mohamed AR, Chan CX, Ragan MA, Zhang J, Cooke I et al. 2019. Close relationship between coral-associated Chromera strains despite major differences within the Symbiodiniaceae. bioRxiv 825992. https://doi.org/10.1101/825992
    [Crossref]
  25. 25.
    González-Pech RA, Stephens TG, Chen Y, Mohamed AR, Cheng Y et al. 2021. Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium. BMC Biol. 19:73
    [Google Scholar]
  26. 26.
    Nand A, Zhan Y, Salazar OR, Aranda M, Voolstra CR, Dekker J. 2021. Genetic and spatial organization of the unusual chromosomes of the dinoflagellate Symbiodinium microadriaticum. Nat. Genet. 53:618–29
    [Google Scholar]
  27. 27.
    Planes S, Allemand D, Agostini S, Banaigs B, Boissin E et al. 2019. The Tara Pacific Expedition—a pan-ecosystemic approach of the “-omics” complexity of coral reef holobionts across the Pacific Ocean. PLOS Biol. 17:e3000483
    [Google Scholar]
  28. 28.
    Cleves PA, Shumaker A, Lee J, Putnam HM, Bhattacharya D. 2020. Unknown to known: advancing knowledge of coral gene function. Trends Genet. 36:93–104
    [Google Scholar]
  29. 29.
    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 476:320–23
    [Google Scholar]
  30. 30.
    Ying H, Hayward DC, Cooke I, Wang W, Moya A et al. 2019. The whole-genome sequence of the coral Acropora millepora. Genome Biol. Evol. 11:1374–79
    [Google Scholar]
  31. 31.
    Shumaker A, Putnam HM, Qiu H, Price DC, Zelzion E et al. 2019. Genome analysis of the rice coral Montipora capitata. Sci. Rep. 9:2571
    [Google Scholar]
  32. 32.
    Helmkampf M, Bellinger MR, Geib SM, Sim SB, Takabayashi M. 2019. Draft genome of the rice coral Montipora capitata obtained from linked-read sequencing. Genome Biol. Evol. 11:2045–54
    [Google Scholar]
  33. 33.
    Celis JS, Wibberg D, Ramrez-Portilla C, Rupp O, Sczyrba A et al. 2018. Binning enables efficient host genome reconstruction in cnidarian holobionts. GigaScience 7:giy075
    [Google Scholar]
  34. 34.
    Bongaerts P, Cooke IR, Ying H, Wels D, den Haan S et al. 2021. Morphological stasis masks ecologically divergent coral species on tropical reefs. Curr. Biol. 31:2286–98
    [Google Scholar]
  35. 35.
    Ying H, Cooke I, Sprungala S, Wang W, Hayward DC et al. 2018. Comparative genomics reveals the distinct evolutionary trajectories of the robust and complex coral lineages. Genome Biol. 19:175
    [Google Scholar]
  36. 36.
    Prada C, Hanna B, Budd AF, Woodley CM, Schmutz J et al. 2016. Empty niches after extinctions increase population sizes of modern corals. Curr. Biol. 26:3190–94
    [Google Scholar]
  37. 37.
    Stephens TG, Strand EL, Mohamed AR, Williams A, Chiles EN et al. 2021. Ploidy variation and its implications for reproduction and population dynamics in two sympatric Hawaiian coral species. bioRxiv 10.1101/2021.11.21.469467. https://doi.org/10.1101/2021.11.21.469467
    [Crossref]
  38. 38.
    Cunning R, Bay R, Gillette P, Baker AC, Traylor-Knowles N. 2018. Comparative analysis of the Pocillopora damicornis genome highlights role of immune system in coral evolution. Sci. Rep. 8:16134
    [Google Scholar]
  39. 39.
    Buitrago-López C, Mariappan KG, Cárdenas A, Gegner HM, Voolstra CR. 2020. The genome of the cauliflower coral Pocillopora verrucosa. Genome Biol. Evol. 12:1911–17
    [Google Scholar]
  40. 40.
    Voolstra CR, Li Y, Liew YJ, Baumgarten S, Zoccola D et al. 2017. Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals. Sci. Rep. 7:17583
    [Google Scholar]
  41. 41.
    Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–12
    [Google Scholar]
  42. 42.
    Stephens TG, Strand EL, Mohamed AR, Williams A, Chiles EN et al. 2021. Ploidy variation and its implications for reproduction and population dynamics in two sympatric Hawaiian coral species. bioRxiv 10.1101/2021.11.21.469467v2. https://www.biorxiv.org/content/10.1101/2021.11.21.469467v2
  43. 43.
    Freudenthal H. 1962. Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J. Protozool. 9:45–52
    [Google Scholar]
  44. 44.
    Pochon X, Putnam HM, Burki F, Gates RD. 2012. Identifying and characterizing alternative molecular markers for the symbiotic and free-living dinoflagellate genus Symbiodinium. PLOS ONE 7:e29816
    [Google Scholar]
  45. 45.
    LaJeunesse TC. 2001. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J. Phycol. 37:866–80
    [Google Scholar]
  46. 46.
    Santos SR, Gutierrez-Rodriguez C, Coffroth MA. 2003. Phylogenetic identification of symbiotic dinoflagellates via length heteroplasmy in domain V of chloroplast large subunit (cp23S)—ribosomal DNA sequences. Mar. Biotechnol. 5:130–40
    [Google Scholar]
  47. 47.
    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
    [Google Scholar]
  48. 48.
    Liu H, Stephens TG, González-Pech RA, Beltran VH, Lapeyre B et al. 2018. Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun. Biol. 1:95
    [Google Scholar]
  49. 49.
    LaJeunesse TC, Lambert G, Andersen RA, Coffroth MA, Galbraith DW. 2005. Symbiodinium (pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates 1. J. Phycol. 41:880–86
    [Google Scholar]
  50. 50.
    Krueger T, Gates RD. 2012. Cultivating endosymbionts—host environmental mimics support the survival of Symbiodinium c15 ex hospite. J. Exp. Mar. Biol. Ecol. 413:169–76
    [Google Scholar]
  51. 51.
    Ros M, Camp EF, Hughes DJ, Crosswell JR, Warner ME et al. 2020. Unlocking the black-box of inorganic carbon-uptake and utilization strategies among coral endosymbionts (Symbiodiniaceae). Limnol. Oceanogr. 65:1747–63
    [Google Scholar]
  52. 52.
    Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. 2016. Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol. 17:132
    [Google Scholar]
  53. 53.
    Shoguchi E, Beedessee G, Tada I, Hisata K, Kawashima T et al. 2018. Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes. BMC Genom. 19:458
    [Google Scholar]
  54. 54.
    Shoguchi E, Beedessee G, Hisata K, Tada I, Narisoko H et al. 2021. A new dinoflagellate genome illuminates a conserved gene cluster involved in sunscreen biosynthesis. Genome Biol. Evol. 13:evaa235
    [Google Scholar]
  55. 55.
    Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O et al. 2016. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci. Rep. 6:39734
    [Google Scholar]
  56. 56.
    Reich HG, Kitchen SA, Stankiewicz KH, Devlin-Durante M, Fogarty ND, Baums IB. 2021. Genomic variation of an endosymbiotic dinoflagellate (Symbiodinium “fitti”) among closely related coral hosts. Mol. Ecol. 30:143500–14
    [Google Scholar]
  57. 57.
    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]
  58. 58.
    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. 53:613–17
    [Google Scholar]
  59. 59.
    Lin S, Song B, Morse D 2021. Spatial organization of dinoflagellate genomes: novel insights and remaining critical questions. J. Phycol. 57:61674–78
    [Google Scholar]
  60. 60.
    Chen Y, González-Pech RA, Stephens TG, Bhattacharya D, Chan CX. 2020. Evidence that inconsistent gene prediction can mislead analysis of dinoflagellate genomes. J. Phycol. 56:6–10
    [Google Scholar]
  61. 61.
    Berkelmans R, Van Oppen MJ. 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 273:2305–12
    [Google Scholar]
  62. 62.
    Jones AM, Berkelmans R, van Oppen MJ, Mieog JC, Sinclair W. 2008. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc. R. Soc. B 275:1359–65
    [Google Scholar]
  63. 63.
    LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT et al. 2010. Host–symbiont recombination versus natural selection in the response of coral–dinoflagellate symbioses to environmental disturbance. Proc. R. Soc. B 277:2925–34
    [Google Scholar]
  64. 64.
    Baumgarten S, Bayer T, Aranda M, Liew YJ, Carr A et al. 2013. Integrating microRNA and mRNA expression profiling in Symbiodinium microadriaticum, a dinoflagellate symbiont of reef-building corals. BMC Genom. 14:704
    [Google Scholar]
  65. 65.
    Krediet CJ, Ritchie KB, Paul VJ, Teplitski M 2013. Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc. R. Soc. B 280:20122328
    [Google Scholar]
  66. 66.
    Apprill A, Weber LG, Santoro AE. 2016. Distinguishing between microbial habitats unravels ecological complexity in coral microbiomes. mSystems 1:e00143–16
    [Google Scholar]
  67. 67.
    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]
  68. 68.
    Sweet M, Croquer A, Bythell J. 2011. Bacterial assemblages differ between compartments within the coral holobiont. Coral Reefs 30:39–52
    [Google Scholar]
  69. 69.
    Rosenberg E, Falkovitz L. 2004. The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annu. Rev. Microbiol. 58:143–159
    [Google Scholar]
  70. 70.
    Hernandez-Agreda A, Gates RD, Ainsworth TD. 2017. Defining the core microbiome in corals’ microbial soup. Trends Microbiol. 25:125–40
    [Google Scholar]
  71. 71.
    Muller EM, Bartels E, Baums IB. 2018. Bleaching causes loss of disease resistance within the threatened coral species Acropora cervicornis. eLife 7:e35066
    [Google Scholar]
  72. 72.
    Ainsworth TD, Krause L, Bridge T, Torda G, Raina JB et al. 2015. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9:2261–74
    [Google Scholar]
  73. 73.
    Hester ER, Barott KL, Nulton J, Vermeij MJ, Rohwer FL. 2016. Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J. 10:1157–69
    [Google Scholar]
  74. 74.
    Neave MJ, Rachmawati R, Xun L, Michell CT, Bourne DG et al. 2017. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. 11:186–200
    [Google Scholar]
  75. 75.
    Neave MJ, Apprill A, Ferrier-Pagès C, Voolstra CR. 2016. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100:8315–24
    [Google Scholar]
  76. 76.
    Bayer T, Neave MJ, Alsheikh-Hussain A, Aranda M, Yum LK et al. 2013. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl. Environ. Microbiol. 79:4759–62
    [Google Scholar]
  77. 77.
    Neave MJ, Michell CT, Apprill A, Voolstra CR. 2014. Whole-genome sequences of three symbiotic endozoicomonas strains. Genome Announc. 2:e00802–14
    [Google Scholar]
  78. 78.
    Bergman JL, Leggat W, Ainsworth TD. 2021. The meta-organism response of the environmental generalist Pocillopora damicornis exposed to differential accumulation of heat stress. Front. Mar. Sci. 8:664063
    [Google Scholar]
  79. 79.
    Haydon TD, Seymour JR, Raina JB, Edmondson J, Siboni N et al. 2021. Rapid shifts in bacterial communities and homogeneity of symbiodiniaceae in colonies of Pocillopora acuta transplanted between reef and mangrove environments. Front. Microbiol. 12:756091
    [Google Scholar]
  80. 80.
    Sweet M, Villela H, Keller-Costa T, Costa R, Romano S et al. 2020. Insights into the cultured bacterial fraction of corals. mSystems 6:e01249–20
    [Google Scholar]
  81. 81.
    Fine M, Loya Y. 2002. Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proc. R. Soc. Lond. B 269:1205–10
    [Google Scholar]
  82. 82.
    Levin RA, Voolstra CR, Weynberg KD, Van Oppen MJH. 2017. Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. ISME J. 11:808–12
    [Google Scholar]
  83. 83.
    Kumar L, Brenner N, Sledzieski S, Olaosebikan M, Lynn-Goin M et al. 2021. Transfer of knowledge from model organisms to evolutionarily distant non-model organisms: the coral Pocillopora damicornis membrane signaling receptome. bioRxiv 10.1101/2021.10.18.464760. https://doi.org/10.1101/2021.10.18.464760
    [Crossref]
  84. 84.
    Remmert M, Biegert A, Hauser A, Söding J. 2012. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat. Methods 9:173–75
    [Google Scholar]
  85. 85.
    Cleves PA, Strader ME, Bay LK, Pringle JR, Matz MV. 2018. CRISPR/Cas9-mediated genome editing in a reef-building coral. PNAS 115:5235–40
    [Google Scholar]
  86. 86.
    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 117:28899–905
    [Google Scholar]
  87. 87.
    Sledzieski S, Singh R, Cowen L, Berger B. 2021. D-SCRIPT translates genome to phenome with sequence-based, structure-aware, genome-scale predictions of protein-protein interactions. Cell Syst. 12:10969–82.e6
    [Google Scholar]
  88. 88.
    Thurber RLV, Barott KL, Hall D, Liu H, Rodriguez-Mueller B et al. 2008. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. PNAS 105:18413–18
    [Google Scholar]
  89. 89.
    Thurber RV, Willner-Hall D, Rodriguez-Mueller B, Desnues C, Edwards RA et al. 2009. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11:2148–63
    [Google Scholar]
  90. 90.
    Wegley L, Edwards R, Rodriguez-Brito B, Liu H, Rohwer F. 2007. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9:2707–19
    [Google Scholar]
  91. 91.
    Messyasz A, Rosales SM, Mueller RS, Sawyer T, Correa A et al. 2020. Coral bleaching phenotypes associated with differential abundances of nucleocytoplasmic large DNA viruses. Front. Mar. Sci. 7:789
    [Google Scholar]
  92. 92.
    Johnson MD, Scott JJ, Leray M, Lucey N, Bravo LMR et al. 2021. Rapid ecosystem-scale consequences of acute deoxygenation on a Caribbean coral reef. Nat. Commun. 12:4522
    [Google Scholar]
  93. 93.
    Cissell EC, McCoy SJ. 2021. Shotgun metagenomic sequencing reveals the full taxonomic, trophic, and functional diversity of a coral reef benthic cyanobacterial mat from Bonaire, Caribbean Netherlands. Sci. Total Environ. 755:142719
    [Google Scholar]
  94. 94.
    Wang Z, Gerstein M, Snyder M. 2009. RNA-seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10:57–63
    [Google Scholar]
  95. 95.
    Lohman BK, Weber JN, Bolnick DI. 2016. Evaluation of TagSeq, a reliable low-cost alternative for RNA seq. Mol. Ecol. Resour. 16:1315–21
    [Google Scholar]
  96. 96.
    Meyer E, Aglyamova G, Matz M. 2011. Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure. Mol. Ecol. 20:3599–616
    [Google Scholar]
  97. 97.
    Connelly MT, McRae CJ, Liu PJ, Traylor-Knowles N. 2020. Lipopolysaccharide treatment stimulates Pocillopora coral genotype-specific immune responses but does not alter coral-associated bacteria communities. Dev. Comp. Immunol. 109:103717
    [Google Scholar]
  98. 98.
    DeSalvo M, Voolstra CR, Sunagawa S, Schwarz J, Stillman J et al. 2008. Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol. Ecol. 17:3952–71
    [Google Scholar]
  99. 99.
    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. 2:140214
    [Google Scholar]
  100. 100.
    Kenkel CD, Matz MV. 2016. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 1:14
    [Google Scholar]
  101. 101.
    Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR. 2013. Genomic basis for coral resilience to climate change. PNAS 110:1387–92
    [Google Scholar]
  102. 102.
    Kelley ER, Sleith RS, Matz MV, Wright RM. 2021. Gene expression associated with disease resistance and long-term growth in a reef-building coral. R. Soc. Open Sci. 8:210113
    [Google Scholar]
  103. 103.
    Granados-Cifuentes C, Bellantuono AJ, Ridgway T, Hoegh-Guldberg O, Rodriguez-Lanetty M. 2013. High natural gene expression variation in the reef-building coral Acropora millepora: potential for acclimative and adaptive plasticity. BMC Genom. 14:228
    [Google Scholar]
  104. 104.
    Dobin A, Gingeras TR. 2015. Mapping RNA-seq reads with STAR. Curr. Protoc. Bioinformatics 51:111419
    [Google Scholar]
  105. 105.
    Bray NL, Pimentel H, Melsted P, Pachter L. 2016. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34:525–27
    [Google Scholar]
  106. 106.
    Seppey M, Manni M, Zdobnov EM 2019. BUSCO: assessing genome assembly and annotation completeness. Gene Prediction M Kollmar 227–45 New York: Humana
    [Google Scholar]
  107. 107.
    Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM. 2021. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol. Biol. Evol. 38:104647–54
    [Google Scholar]
  108. 108.
    Shinzato C, Inoue M, Kusakabe M. 2014. A snapshot of a coral “holobiont”: a transcriptome assembly of the scleractinian coral, porites, captures a wide variety of genes from both the host and symbiotic zooxanthellae. PLOS ONE 9:e85182
    [Google Scholar]
  109. 109.
    Eirin-Lopez JM, Putnam HM. 2019. Marine environmental epigenetics. Annu. Rev. Mar. Sci. 11:335–68
    [Google Scholar]
  110. 110.
    Dixon GB, Bay LK, Matz MV. 2014. Bimodal signatures of germline methylation are linked with gene expression plasticity in the coral Acropora millepora. BMC Genom. 15:1109
    [Google Scholar]
  111. 111.
    Dimond JL, Roberts SB. 2016. Germline DNA methylation in reef corals: patterns and potential roles in response to environmental change. Mol. Ecol. 25:1895–904
    [Google Scholar]
  112. 112.
    Putnam HM, Davidson JM, Gates RD. 2016. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol. Appl. 9:1165–78
    [Google Scholar]
  113. 113.
    Dixon G, Liao Y, Bay LK, Matz MV. 2018. Role of gene body methylation in acclimatization and adaptation in a basal metazoan. PNAS 115:13342–46
    [Google Scholar]
  114. 114.
    Liew YJ, Zoccola D, Li Y, Tambutté E, Venn AA et al. 2018. Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral. Sci. Adv. 4:eaar8028
    [Google Scholar]
  115. 115.
    Dixon G, Matz M. 2021. Benchmarking DNA methylation assays in a reef-building coral. Mol. Ecol. Resour. 21:464–77
    [Google Scholar]
  116. 116.
    Trigg SA, Venkataraman YR, Gavery M, Roberts SB, Bhattacharya D et al. 2021. Invertebrate methylomes provide insight into mechanisms of environmental tolerance and reveal methodological biases. Mol. Ecol. Resour. 22:41247–61
    [Google Scholar]
  117. 117.
    Rodriguez-Casariego JA, Ladd MC, Shantz AA, Lopes C, Cheema MS et al. 2018. Coral epigenetic responses to nutrient stress: Histone H2A.X phosphorylation dynamics and DNA methylation in the staghorn coral Acropora cervicornis. Ecol. Evol. 8:12193–207
    [Google Scholar]
  118. 118.
    Dimond JL, Roberts SB. 2020. Convergence of DNA methylation profiles of the reef coral Porites astreoides in a novel environment. Front. Mar. Sci. 6:792
    [Google Scholar]
  119. 119.
    Rodriguez-Casariego JA, Cunning R, Baker AC, Eirin-Lopez JM. 2021. Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa. Mol. Ecol. 31:2588–602
    [Google Scholar]
  120. 120.
    Liew YJ, Howells EJ, Wang X, Michell CT, Burt JA et al. 2020. Intergenerational epigenetic inheritance in reef-building corals. Nat. Climate Change 10:254–59
    [Google Scholar]
  121. 121.
    Li Y, Liew YJ, Cui G, Cziesielski MJ, Zahran N et al. 2018. DNA methylation regulates transcriptional homeostasis of algal endosymbiosis in the coral model Aiptasia. Sci. Adv. 4:eaat2142
    [Google Scholar]
  122. 122.
    Weizman E, Levy O. 2019. The role of chromatin dynamics under global warming response in the symbiotic coral model Aiptasia. Commun. Biol. 2:282
    [Google Scholar]
  123. 123.
    Adrian-Kalchhauser I, Sultan SE, Shama LN, Spence-Jones H, Tiso S et al. 2020. Understanding ‘non-genetic’ inheritance: insights from molecular-evolutionary crosstalk. Trends Ecol. Evol. 35:121078–89
    [Google Scholar]
  124. 124.
    Drake JL, Mass T, Haramaty L, Zelzion E, Bhattacharya D, Falkowski PG. 2013. Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata. PNAS 110:3788–93
    [Google Scholar]
  125. 125.
    Ramos-Silva P, Kaandorp J, Huisman L, Marie B, Zanella-Cléon I et al. 2013. The skeletal proteome of the coral Acropora millepora: the evolution of calcification by co-option and domain shuffling. Mol. Biol. Evol. 30:2099–112
    [Google Scholar]
  126. 126.
    Takeuchi T, Yamada L, Shinzato C, Sawada H, Satoh N. 2016. Stepwise evolution of coral biomineralization revealed with genome-wide proteomics and transcriptomics. PLOS ONE 11:e0156424
    [Google Scholar]
  127. 127.
    Drake JL, Whitelegge JP, Jacobs DK. 2020. First sequencing of ancient coral skeletal proteins. Sci. Rep. 10:19407
    [Google Scholar]
  128. 128.
    Ricaurte M, Schizas NV, Ciborowski P, Boukli NM. 2016. Proteomic analysis of bleached and unbleached Acropora palmata, a threatened coral species of the Caribbean. Mar. Pollut. Bull. 107:224–32
    [Google Scholar]
  129. 129.
    Petrou K, Nunn B, Padula M, Miller D, Nielsen D. 2021. Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora. Sci. Rep. 11:19061
    [Google Scholar]
  130. 130.
    Tortorelli G, Oakley CA, Davy SK, van Oppen MJ, McFadden GI. 2021. Cell wall proteomic analysis of the cnidarian photosymbionts Breviolum minutum and Cladocopium goreaui. J. Eukaryot. Microbiol. 69:1e12870
    [Google Scholar]
  131. 131.
    Wong YH, Zhang Y, Lun JC, Qiu JW. 2021. A proteomic analysis of skeletal tissue anomaly in the brain coral Platygyra carnosa. Mar. Pollut. Bull. 164:111982
    [Google Scholar]
  132. 132.
    Tisthammer KH, Timmins-Schiffman E, Seneca FO, Nunn BL, Richmond RH. 2021. Physiological and molecular responses of lobe coral indicate nearshore adaptations to anthropogenic stressors. Sci. Rep. 11:3423
    [Google Scholar]
  133. 133.
    Cheng H, Zhao H, Yang T, Ruan S, Wang H et al. 2018. Comparative evaluation of five protocols for protein extraction from stony corals (Scleractinia) for proteomics. Electrophoresis 39:1062–70
    [Google Scholar]
  134. 134.
    Sogin EM, Putnam HM, Anderson PE, Gates RD. 2016. Metabolomic signatures of increases in temperature and ocean acidification from the reef-building coral, Pocillopora damicornis. Metabolomics 12:71
    [Google Scholar]
  135. 135.
    Sogin EM, Putnam HM, Nelson CE, Anderson P, Gates RD. 2017. Correspondence of coral holobiont metabolome with symbiotic bacteria, archaea and Symbiodinium communities. Environ. Microbiol. Rep. 9:310–15
    [Google Scholar]
  136. 136.
    Stien D, Suzuki M, Rodrigues AM, Yvin M, Clergeaud F et al. 2020. A unique approach to monitor stress in coral exposed to emerging pollutants. Sci. Rep. 10:9601
    [Google Scholar]
  137. 137.
    Hillyer KE, Dias DA, Lutz A, Wilkinson SP, Roessner U, Davy SK. 2017. Metabolite profiling of symbiont and host during thermal stress and bleaching in the coral Acropora aspera. Coral Reefs 36:105–18
    [Google Scholar]
  138. 138.
    Hillyer KE, Dias D, Lutz A, Roessner U, Davy SK. 2018. 13C metabolomics reveals widespread change in carbon fate during coral bleaching. Metabolomics 14:12
    [Google Scholar]
  139. 139.
    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 114:13194–99
    [Google Scholar]
  140. 140.
    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 285:20182336
    [Google Scholar]
  141. 141.
    Matthews JL, Cunning R, Ritson-Williams R, Oakley CA, Lutz A et al. 2020. Metabolite pools of the reef building coral Montipora capitata are unaffected by Symbiodiniaceae community composition. Coral Reefs 39:1727–37
    [Google Scholar]
  142. 142.
    Andersson ER, Day RD, Work TM, Anderson PE, Woodley CM, Schock TB. 2021. Identifying metabolic alterations associated with coral growth anomalies using 1H NMR metabolomics. Coral Reefs 40:1195–209
    [Google Scholar]
  143. 143.
    Roach TN, Dilworth J, Jones AD, Quinn RA, Drury C et al. 2021. Metabolomic signatures of coral bleaching history. Nat. Ecol. Evol. 5:495–503
    [Google Scholar]
  144. 144.
    Williams A, Pathmanathan JS, Stephens TG, Su X, Chiles EN et al. 2021. Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata. PeerJ 9:e12335
    [Google Scholar]
  145. 145.
    Cziesielski MJ, Liew YJ, Cui G, Schmidt-Roach S, Campana S et al. 2018. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc. R. Soc. B 285:20172654
    [Google Scholar]
  146. 146.
    Falkowski PG, Dubinsky Z, Muscatine L, Porter JW. 1984. Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–9
    [Google Scholar]
  147. 147.
    Muscatine L, McCloskey LR, Marian RE 1981. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 26:601–11
    [Google Scholar]
  148. 148.
    Veron JE, Hoegh-Guldberg O, Lenton TM, Lough JM, Obura DO et al. 2009. The coral reef crisis: the critical importance of <350 ppm CO2. Mar. Pollut. Bull. 58:1428–36
    [Google Scholar]
  149. 149.
    Brown B. 1997. Coral bleaching: causes and consequences. Coral Reefs 16:S129–38
    [Google Scholar]
  150. 150.
    Burt J, Al-Harthi S, Al-Cibahy A. 2011. Long-term impacts of coral bleaching events on the world's warmest reefs. Mar. Environ. Res. 72:225–29
    [Google Scholar]
  151. 151.
    Graham N, Nash K, Kool J. 2011. Coral reef recovery dynamics in a changing world. Coral Reefs 30:283–94
    [Google Scholar]
  152. 152.
    Hughes TP, Graham NA, Jackson JB, Mumby PJ, Steneck RS. 2010. Rising to the challenge of sustaining coral reef resilience. Trends Ecol. Evol. 25:633–42
    [Google Scholar]
  153. 153.
    Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333:418–22
    [Google Scholar]
  154. 154.
    Cheung MW, Hock K, Skirving W, Mumby PJ. 2021. Cumulative bleaching undermines systemic resilience of the Great Barrier Reef. Curr. Biol. 31:235385–92.e4
    [Google Scholar]
  155. 155.
    Shpilker P, Freeman J, McKelvie H, Ashey J, Fonticella JM et al. 2021. MEtaData Format for Open Reef Data (MEDFORD). Metadata and Semantic Research: 15th International Conference, MTSR 2021, Virtual Event, November 29 – December 3, 2021, Revised Selected Papersed. E Garoufallou, MA Ovalle-Perandones, A Vlachidispp. 20611 Berlin: Springer
    [Google Scholar]
  156. 156.
    Hume BC, Voolstra CR, Arif C, D'Angelo C, Burt JA et al. 2016. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to holocene climate change. PNAS 113:4416–21
    [Google Scholar]
  157. 157.
    Van Oppen MJH, Lough JM, eds. 2008. Coral Bleaching Berlin: Springer
    [Google Scholar]
  158. 158.
    Buddemeier RW, Baker AC, Fautin DG, Jacobs JR 2004. The adaptive hypothesis of bleaching. Coral Health and Disease E Rosenberg, Y Loya 427–44 Berlin: Springer
    [Google Scholar]
  159. 159.
    Morgans CA, Hung JY, Bourne DG, Quigley KM. 2020. Symbiodiniaceae probiotics for use in bleaching recovery. Restor. Ecol. 28:282–88
    [Google Scholar]
  160. 160.
    Buerger P, Alvarez-Roa C, Coppin C, Pearce S, Chakravarti L et al. 2020. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci. Adv. 6:eaba2498
    [Google Scholar]
  161. 161.
    Chakravarti LJ, van Oppen MJ. 2018. Experimental evolution in coral photosymbionts as a tool to increase thermal tolerance. Front. Mar. Sci. 5:227
    [Google Scholar]
  162. 162.
    Coffroth MA, Poland DM, Petrou EL, Brazeau DA, Holmberg JC. 2010. Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals. PLOS ONE 5:e13258
    [Google Scholar]
  163. 163.
    Rodrigues LJ, Grottoli AG. 2007. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr. 52:1874–82
    [Google Scholar]
  164. 164.
    Bruno JF, Selig ER, Casey KS, Page CA, Willis BL et al. 2007. Thermal stress and coral cover as drivers of coral disease outbreaks. PLOS Biol. 5:e124
    [Google Scholar]
  165. 165.
    Santoro EP, Borges RM, Espinoza JL, Freire M, Messias CS et al. 2021. Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Sci. Adv. 7:eabg3088
    [Google Scholar]
  166. 166.
    Shilling EN, Combs IR, Voss JD. 2021. Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa. Sci. Rep. 11:8566
    [Google Scholar]
  167. 167.
    Sweet MJ, Séré MG. 2016. Ciliate communities consistently associated with coral diseases. J. Sea Res. 113:119–31
    [Google Scholar]
  168. 168.
    Mera H, Bourne DG. 2018. Disentangling causation: complex roles of coral-associated microorganisms in disease. Environ. Microbiol. 20:431–49
    [Google Scholar]
  169. 169.
    Moriarty T, Leggat W, Huggett MJ, Ainsworth T. 2020. Coral disease causes, consequences, and risk within coral restoration. Trends Microbiol. 28:793–807
    [Google Scholar]
  170. 170.
    Peters EC 2015. Diseases of coral reef organisms. Coral Reefs in the Anthropocene C Birkeland 147–78 Dordrecht, Neth: Springer Sci. Bus. Media
    [Google Scholar]
  171. 171.
    Rosenberg E, Loya Y, eds. 2013. Coral Health and Disease Berlin: Springer
    [Google Scholar]
  172. 172.
    Becker CC, Brandt M, Miller CA, Apprill A. 2022. Microbial bioindicators of Stony Coral Tissue Loss Disease identified in corals and overlying waters using a rapid field-based sequencing approach. Environ. Microbiol. 24:3116682
    [Google Scholar]
  173. 173.
    Meiling SS, Muller EM, Lasseigne D, Rossin A, Veglia AJ et al. 2021. Variable species responses to experimental stony coral tissue loss disease (SCTLD) exposure. Front. . Mar. Sci. 8:670829
    [Google Scholar]
  174. 174.
    Meyer JL, Castellanos-Gell J, Aeby GS, Häse CC, Ushijima B, Paul VJ. 2019. Microbial community shifts associated with the ongoing stony coral tissue loss disease outbreak on the Florida Reef Tract. Front. Microbiol. 10:2244
    [Google Scholar]
  175. 175.
    Rosales SM, Clark AS, Huebner LK, Ruzicka RR, Muller EM. 2020. Rhodobacterales and Rhizobiales are associated with stony coral tissue loss disease and its suspected sources of transmission. Front. Microbiol. 11:681
    [Google Scholar]
  176. 176.
    Ritchie KB. 2006. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322:1–14
    [Google Scholar]
  177. 177.
    McDevitt-Irwin JM, Baum JK, Garren M, Vega Thurber RL. 2017. Responses of coral-associated bacterial communities to local and global stressors. Front. Mar. Sci. 4:262
    [Google Scholar]
  178. 178.
    Zaneveld JR, Burkepile DE, Shantz AA, Pritchard CE, McMinds R et al. 2016. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun. 7:11833
    [Google Scholar]
  179. 179.
    Ainsworth TD, Gates RD. 2016. Corals' microbial sentinels. Science 352:1518–19
    [Google Scholar]
  180. 180.
    Van Oppen MJ, Oliver JK, Putnam HM, Gates RD. 2015. Building coral reef resilience through assisted evolution. PNAS 112:2307–13
    [Google Scholar]
  181. 181.
    Anthony K, Bay LK, Costanza R, Firn J, Gunn J et al. 2017. New interventions are needed to save coral reefs. Nat. Ecol. Evol. 1:1420–22
    [Google Scholar]
  182. 182.
    Mayfield AB, Tsai S, Lin C. 2019. The coral hospital. Biopreserv. Biobank. 17:355–69
    [Google Scholar]
  183. 183.
    Baums IB. 2008. A restoration genetics guide for coral reef conservation. Mol. Ecol. 17:2796–811
    [Google Scholar]
  184. 184.
    Louis YD, Bhagooli R, Kenkel CD, Baker AC, Dyall SD. 2017. Gene expression biomarkers of heat stress in scleractinian corals: promises and limitations. Comp. Biochem. Physiol. C 191:63–77
    [Google Scholar]
  185. 185.
    Kenkel CD, Aglyamova G, Alamaru A, Bhagooli R, Capper R et al. 2011. Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites. PLOS ONE 6:e26914
    [Google Scholar]
  186. 186.
    Kenkel C, Sheridan C, Leal M, Bhagooli R, Castillo K et al. 2014. Diagnostic gene expression biomarkers of coral thermal stress. Mol. Ecol. Resour. 14:667–78
    [Google Scholar]
  187. 187.
    Traylor-Knowles N, Palumbi SR. 2014. Translational environmental biology: cell biology informing conservation. Trends Cell Biol. 24:265–67
    [Google Scholar]
  188. 188.
    Dias M, Madeira C, Jogee N, Ferreira A, Gouveia R et al. 2020. Integrative indices for health assessment in reef corals under thermal stress. Ecol. Indicators 113:106230
    [Google Scholar]
  189. 189.
    Bay RA, Palumbi SR. 2015. Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biol. Evol. 7:1602–12
    [Google Scholar]
  190. 190.
    Parkinson JE, Bartels E, Devlin-Durante MK, Lustic C, Nedimyer K et al. 2018. Extensive transcriptional variation poses a challenge to thermal stress biomarker development for endangered corals. Mol. Ecol. 27:1103–19
    [Google Scholar]
  191. 191.
    Putnam HM. 2021. Avenues of reef-building coral acclimatization in response to rapid environmental change. J. Exp. Biol. 224:jeb239319
    [Google Scholar]
  192. 192.
    Brown BE, Dunne RP, Goodson M, Douglas A. 2000. Bleaching patterns in reef corals. Nature 404:142–43
    [Google Scholar]
  193. 193.
    Brown BE, Dunne RP, Edwards AJ, Sweet MJ, Phongsuwan N. 2015. Decadal environmental ‘memory’ in a reef coral?. Mar. Biol. 162:479–83
    [Google Scholar]
  194. 194.
    Majerova E, Carey FC, Drury C, Gates RD. 2021. Preconditioning improves bleaching tolerance in the reef-building coral Pocillopora acuta through modulations in the programmed cell death pathways. Mol. Ecol. 30:143560–74
    [Google Scholar]
  195. 195.
    Bellantuono AJ, Granados-Cifuentes C, Miller DJ, Hoegh-Guldberg O, Rodriguez-Lanetty M. 2012. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLOS ONE 7:e50685
    [Google Scholar]
  196. 196.
    Putnam HM, Ritson-Williams R, Cruz JA, Davidson JM, Gates RD. 2020. Environmentally-induced parental or developmental conditioning influences coral offspring ecological performance. Sci. Rep. 10:13664
    [Google Scholar]
  197. 197.
    Putnam HM, Gates RD. 2015. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J. Exp. Biol. 218:2365–72
    [Google Scholar]
  198. 198.
    Hackerott S, Martell HA, Eirin-Lopez JM. 2021. Coral environmental memory: causes, mechanisms, and consequences for future reefs. Trends Ecol. Evol. 36:111011–23
    [Google Scholar]
  199. 199.
    Shelyakin PV, Garushyants SK, Nikitin MA, Mudrova SV, Berumen M et al. 2018. Microbiomes of gall-inducing copepod crustaceans from the corals Stylophora pistillata (Scleractinia) and Gorgonia ventalina (Alcyonacea). Sci. Rep. 8:11563
    [Google Scholar]
  200. 200.
    Reshef L, Koren O, Loya Y, Zilber-Rosenberg I, Rosenberg E. 2006. The coral probiotic hypothesis. Environ. Microbiol. 8:2068–73
    [Google Scholar]
  201. 201.
    Peixoto RS, Rosado PM, de Assis Leite DC, Rosado AS, Bourne DG. 2017. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8:341
    [Google Scholar]
  202. 202.
    Rosado PM, Leite DC, Duarte GA, Chaloub RM, Jospin G et al. 2019. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J. 13:921–36
    [Google Scholar]
  203. 203.
    Peixoto RS, Sweet M, Villela HD, Cardoso P, Thomas T et al. 2021. Coral probiotics: premise, promise, prospects. Annu. Rev. Anim. Biosci. 9:265–88
    [Google Scholar]
  204. 204.
    Doering T, Wall M, Putchim L, Rattanawongwan T, Schroeder R et al. 2021. Towards enhancing coral heat tolerance: a “microbiome transplantation” treatment using inoculations of homogenized coral tissues. Microbiome 9:102
    [Google Scholar]
  205. 205.
    Cohen Y, Joseph Pollock F, Rosenberg E, Bourne DG. 2013. Phage therapy treatment of the coral pathogen Vibrio coralliilyticus. Microbiologyopen 2:64–74
    [Google Scholar]
  206. 206.
    Lamb JB, Van De Water JA, Bourne DG, Altier C, Hein MY et al. 2017. Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates. Science 355:731–33
    [Google Scholar]
  207. 207.
    Dixon GB, Davies SW, Aglyamova GV, Meyer E, Bay LK, Matz MV. 2015. Genomic determinants of coral heat tolerance across latitudes. Science 348:1460–62
    [Google Scholar]
  208. 208.
    Quigley KM, Bay LK, van Oppen MJ. 2020. Genome-wide SNP analysis reveals an increase in adaptive genetic variation through selective breeding of coral. Mol. Ecol. 29:2176–88
    [Google Scholar]
  209. 209.
    Howells EJ, Abrego D, Liew YJ, Burt JA, Meyer E, Aranda M. 2021. Enhancing the heat tolerance of reef-building corals to future warming. Sci. Adv. 7:eabg6070
    [Google Scholar]
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