A genomic view of the reef-building coral Porites lutea and its microbial symbionts


Corals and the reef ecosystems that they support are in global decline due to increasing anthropogenic pressures such as climate change1. However, effective reef conservation strategies are hampered by a limited mechanistic understanding of coral biology and the functional roles of the diverse microbial communities that underpin coral health2,3. Here, we present an integrated genomic characterization of the coral species Porites lutea and its microbial partners. High-quality genomes were recovered from P. lutea, as well as a metagenome-assembled Cladocopium C15 (the dinoflagellate symbiont) and 52 bacterial and archaeal populations. Comparative genomic analysis revealed that many of the bacterial and archaeal genomes encode motifs that may be involved in maintaining association with the coral host and in supplying fixed carbon, B-vitamins and amino acids to their eukaryotic partners. Furthermore, mechanisms for ammonia, urea, nitrate, dimethylsulfoniopropionate and taurine transformation were identified that interlink members of the holobiont and may be important for nutrient acquisition and retention in oligotrophic waters. Our findings demonstrate the critical and diverse roles that microorganisms play within the coral holobiont and underscore the need to consider all of the components of the holobiont if we are to effectively inform reef conservation strategies.

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Fig. 1: Unscaled phylogenetic tree showing all bacterial and archaeal MAGs (n = 52 MAGs) that were recovered from P. lutea.
Fig. 2: P. lutea MAG statistics and relative abundance as calculated by read mapping.
Fig. 3: Schematic overview of interactions between all of the members of the P. lutea holobiont.

Data availability

All genomic data generated by the Reef Future Genomics consortium, including the P. lutea and seawater MAGs, can be accessed at http://refuge2020.reefgenomics.org. Furthermore, the P. lutea metagenomic reads and MAGs are available at NCBI under the Bioproject accession PRJNA545004. The bacterial and archaeal MAGs from P. lutea have also been deposited in the Integrated Microbial Genomes database (IMG) and IMG accession numbers can be found in Supplementary Table 1. All graftM packages can be found at https://data.ace.uq.edu.au/public/graftm/7/ as well as the GraftM GitHub repository (https://github.com/geronimp/graftM_gpkgs).

Code availability

All code that has not previously been published is available through GitHub (https://github.com/) as cited in the Methods. Code for the following software can be found on their respective GitHub pages: https://github.com/geronimp/enrichM, https://github.com/jstjohn/SeqPrep, https://github.com/Victorian-Bioinformatics-Consortium/nesoni, https://github.com/Ecogenomics/mingle, https://github.com/dparks1134/GeneTreeTk, https://github.com/sylvainforet/libngs, https://github.com/sylvainforet/psytrans, https://github.com/PASApipeline, https://github.com/TransDecoder/TransDecoder/wiki, https://github.com/Ecogenomics/BamM, https://github.com/wwood/CoverM, and https://github.com/dparks1134/UniteM, https://github.com/geronimp/enrichM. The modified scripts of AUGUSTUS and PASA for annotating Cladocopium C15 genome are available at http://smic.reefgenomics.org/download/ and https://github.com/chancx/dinoflag-alt-splice.


  1. 1.

    Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    CAS  PubMed  Google Scholar 

  2. 2.

    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 317–340 (2016).

    CAS  PubMed  Google Scholar 

  3. 3.

    Torda, G. et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7, 627–636 (2017).

    Google Scholar 

  4. 4.

    Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Change 1, 165–169 (2011).

    CAS  Google Scholar 

  5. 5.

    Voolstra, C. R. et al. Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals. Sci. Rep. 7, 17583 (2017).

    PubMed  PubMed Central  Google Scholar 

  6. 6.

    Shinzato, C. et al. Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476, 320–323 (2011).

    CAS  PubMed  Google Scholar 

  7. 7.

    LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580 (2018).

    CAS  PubMed  Google Scholar 

  8. 8.

    LaJeunesse, T. C. et al. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23, 596–603 (2004).

    Google Scholar 

  9. 9.

    Fitt, W. K. et al. Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J. Exp. Mar. Bio. Ecol. 373, 102–110 (2009).

    Google Scholar 

  10. 10.

    Aranda, M. et al. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci. Rep. 6, 39734 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Krueger, T. & Gates, R. D. Cultivating endosymbionts—host environmental mimics support the survival of Symbiodinium C15 ex hospite. J. Exp. Mar. Bio. Ecol. 413, 169–176 (2012).

    Google Scholar 

  12. 12.

    Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 10, 2280–2292 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Pootakham, W. et al. High resolution profiling of coral-associated bacterial communities using full-length 16S rRNA sequence data from PacBio SMRT sequencing system. Sci. Rep. 7, 2774 (2017).

    PubMed  PubMed Central  Google Scholar 

  14. 14.

    Li, J. et al. Bacterial dynamics within the mucus, tissue and skeleton of the coral Porites lutea during different seasons. Sci. Rep. 4, 7320 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Wegley, L., Edwards, R., Rodriguez‐Brito, B., Liu, H. & Rohwer, F. Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ. Microbiol. 9, 2707–2719 (2007).

    CAS  PubMed  Google Scholar 

  16. 16.

    Podell, S. et al. Pangenomic comparison of globally distributed Poribacteria associated with sponge hosts and marine particles. ISME J. 13, 468–481 (2019).

    CAS  PubMed  Google Scholar 

  17. 17.

    Nguyen, M. T. H. D., Liu, M. & Thomas, T. Ankyrin‐repeat proteins from sponge symbionts modulate amoebal phagocytosis. Mol. Ecol. 23, 1635–1645 (2014).

    CAS  PubMed  Google Scholar 

  18. 18.

    Al-Khodor, S., Price, C. T., Kalia, A. & Kwaik, Y. A. Functional diversity of ankyrin repeats in microbial proteins. Trends Microbiol. 18, 132–139 (2010).

    CAS  PubMed  Google Scholar 

  19. 19.

    Jernigan, K. K. & Bordenstein, S. R. Ankyrin domains across the Tree of Life. PeerJ 2, e264 (2014).

    PubMed  PubMed Central  Google Scholar 

  20. 20.

    Xu, C. & Min, J. Structure and function of WD40 domain proteins. Protein Cell 2, 202–214 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Hallam, S. J. et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl Acad. Sci. USA 103, 18296–18301 (2006).

    CAS  PubMed  Google Scholar 

  22. 22.

    Kamke, J. et al. The candidate phylum Poribacteria by single-cell genomics: new insights into phylogeny, cell-compartmentation, eukaryote-like repeat proteins, and other genomic features. PLoS ONE 9, e87353 (2014).

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Yano, K. et al. CERBERUS, a novel U‐box protein containing WD‐40 repeats, is required for formation of the infection thread and nodule development in the legume–Rhizobium symbiosis. Plant J. 60, 168–180 (2009).

    CAS  PubMed  Google Scholar 

  24. 24.

    Tully, B. J., Graham, E. D. & Heidelberg, J. F. The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Sci. Data 5, 170203 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Falkowski, P. G., Dubinsky, Z., Muscatine, L. & Porter, J. W. Light and the bioenergetics of a symbiotic coral. Bioscience 34, 705–709 (1984).

    CAS  Google Scholar 

  26. 26.

    Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189 (2006).

    CAS  PubMed  Google Scholar 

  27. 27.

    Palardy, J. E., Rodrigues, L. J. & Grottoli, A. G. The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. J. Exp. Mar. Bio. Ecol. 367, 180–188 (2008).

    CAS  Google Scholar 

  28. 28.

    Falkowski, P. G., Dubinsky, Z., Muscatine, L. & McCloskey, L. Population control in symbiotic corals: ammonium ions and organic materials maintain the density of zooxanthellae. Bioscience 43, 606–611 (1993).

    Google Scholar 

  29. 29.

    Walker, C. B. et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl Acad. Sci. USA 107, 8818–8823 (2010).

    CAS  PubMed  Google Scholar 

  30. 30.

    Garren, M. & Azam, F. Corals shed bacteria as a potential mechanism of resilience to organic matter enrichment. ISME J. 6, 1159–1165 (2012).

    CAS  PubMed  Google Scholar 

  31. 31.

    Koren, O. & Rosenberg, E. Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl. Environ. Microbiol. 72, 5254–5259 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J. & Smith, A. G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438, 90–93 (2005).

    CAS  PubMed  Google Scholar 

  33. 33.

    Salem, H. et al. Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proc. R. Soc. B 281, 20141838 (2014).

    PubMed  Google Scholar 

  34. 34.

    Shinzato, C., Inoue, M. & Kusakabe, M. 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 (2014).

    PubMed  PubMed Central  Google Scholar 

  35. 35.

    Pogoreutz, C. et al. Sugar enrichment provides evidence for a role of nitrogen fixation in coral bleaching. Glob. Change Biol. 23, 3838–3848 (2017).

    Google Scholar 

  36. 36.

    Pogoreutz, C. et al. Nitrogen fixation aligns with nifH abundance and expression in two coral trophic functional groups. Front. Microbiol. 8, 1187 (2017).

    PubMed  PubMed Central  Google Scholar 

  37. 37.

    Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J. & Wild, C. Nitrogen cycling in corals: the key to understanding holobiont functioning? Trends Microbiol. 23, 490–497 (2015).

    PubMed  Google Scholar 

  38. 38.

    Cardini, U., Bednarz, V. N., Foster, R. A. & Wild, C. Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol. Evol. 4, 1706–1727 (2014).

    PubMed  PubMed Central  Google Scholar 

  39. 39.

    Crandall, J. B. & Teece, M. A. Urea is a dynamic pool of bioavailable nitrogen in coral reefs. Coral Reefs 31, 207–214 (2012).

    Google Scholar 

  40. 40.

    Grover, R., Maguer, J. F., Allemand, D. & Ferrier-Pagès, C. Urea uptake by the scleractinian coral Stylophora pistillata. J. Exp. Mar. Bio. Ecol. 332, 216–225 (2006).

    CAS  Google Scholar 

  41. 41.

    Loya, Y. et al. Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122–131 (2001).

    Google Scholar 

  42. 42.

    Kopp, C. et al. Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen. mBio 4, e00052-13 (2013).

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    Wegley, L. et al. Coral-associated Archaea. Mar. Ecol. Prog. Ser. 273, 89–96 (2004).

    CAS  Google Scholar 

  44. 44.

    Siboni, N., Ben‐Dov, E., Sivan, A. & Kushmaro, A. Global distribution and diversity of coral‐associated Archaea and their possible role in the coral holobiont nitrogen cycle. Environ. Microbiol. 10, 2979–2990 (2008).

    CAS  PubMed  Google Scholar 

  45. 45.

    Siboni, N., Ben-Dov, E., Sivan, A. & Kushmaro, A. Geographic specific coral-associated ammonia-oxidizing archaea in the northern Gulf of Eilat (Red Sea). Microb. Ecol. 64, 18–24 (2012).

    PubMed  Google Scholar 

  46. 46.

    Kellogg, C. A. Tropical Archaea: diversity associated with the surface microlayer of corals. Mar. Ecol. Prog. Ser. 273, 81–88 (2004).

    CAS  Google Scholar 

  47. 47.

    Koch, H. et al. Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc. Natl Acad. Sci. USA 112, 11371–11376 (2015).

    CAS  PubMed  Google Scholar 

  48. 48.

    Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt, E. & Thompson, F. The Prokaryotes: Prokaryotic Communities and Ecophysiology (Springer, 2012).

  49. 49.

    Krapp, A. et al. Nitrate transport and signalling in Arabidopsis. J. Exp. Bot. 65, 789–798 (2014).

    CAS  PubMed  Google Scholar 

  50. 50.

    Raina, J. B. et al. Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria. eLife 6, e23008 (2017).

    PubMed  PubMed Central  Google Scholar 

  51. 51.

    Raina, J.-B. et al. DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502, 677–680 (2013).

    CAS  PubMed  Google Scholar 

  52. 52.

    Curson, A. R. J., Todd, J. D., Sullivan, M. J. & Johnston, A. W. B. Catabolism of dimethylsulphoniopropionate: microorganisms, enzymes and genes. Nat. Rev. Microbiol. 9, 849–859 (2011).

    CAS  PubMed  Google Scholar 

  53. 53.

    Alcolombri, U., Lei, L., Meltzer, D., Vardi, A. & Tawfik, D. S. Assigning the algal source of dimethylsulfide using a selective lyase inhibitor. ACS Chem. Biol. 12, 41–46 (2017).

    CAS  PubMed  Google Scholar 

  54. 54.

    Sunda, W., Kieber, D. J., Kiene, R. P. & Huntsman, S. An antioxidant function for DMSP and DMS in marine algae. Nature 418, 317–320 (2002).

    CAS  PubMed  Google Scholar 

  55. 55.

    Schuller-Levis, G. B. & Park, E. Taurine: new implications for an old amino acid. FEMS Microbiol. Lett. 226, 195–202 (2003).

    CAS  PubMed  Google Scholar 

  56. 56.

    Levin, R. A. et al. Engineering strategies to decode and enhance the genomes of coral symbionts. Front. Microbiol. 8, 1220 (2017).

    PubMed  PubMed Central  Google Scholar 

  57. 57.

    Peixoto, R. S., Rosado, P. M., de Assis Leite, D. C., Rosado, A. S. & Bourne, D. G. Beneficial microorganisms for corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8, 1–16 (2017).

    CAS  Google Scholar 

  58. 58.

    Rosado, P. M. et al. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J. 13, 921–936 (2019).

    CAS  PubMed  Google Scholar 

  59. 59.

    Kwong, W. K., del Campo, J., Mathur, V., Vermeij, M. J. A. & Keeling, P. J. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568, 103–107 (2019).

    CAS  PubMed  Google Scholar 

  60. 60.

    Engelbrektson, A. et al. Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J. 4, 642–647 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Wu, Y.-W., Simmons, B. A. & Singer, S. W. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607 (2016).

    CAS  PubMed  Google Scholar 

  63. 63.

    Kang, D. D., Froula, J., Egan, R. & Wang, Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3, e1165 (2015).

    PubMed  PubMed Central  Google Scholar 

  64. 64.

    Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Evans, P. N. et al. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science 350, 434–438 (2015).

    CAS  PubMed  Google Scholar 

  66. 66.

    McDonald, D. et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610–618 (2012).

    CAS  PubMed  Google Scholar 

  67. 67.

    Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Boratyn, G. M. et al. BLAST: a more efficient report with usability improvements. Nucleic Acids Res. 41, 29–33 (2013).

    Google Scholar 

  69. 69.

    Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. DRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Boyd, J. A., Woodcroft, B. J. & Tyson, G. W. GraftM: a tool for scalable, phylogenetically informed classification of genes within metagenomes. Nucleic Acids Res. 46, e59 (2018).

    PubMed  PubMed Central  Google Scholar 

  71. 71.

    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).

    PubMed  PubMed Central  Google Scholar 

  72. 72.

    Howard, E. C., Sun, S., Biers, E. J. & Moran, M. A. Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ. Microbiol. 10, 2397–2410 (2008).

    CAS  PubMed  Google Scholar 

  73. 73.

    Howard, E. C. et al. Bacterial taxa that limis sulphur flux from the ocean. Science 314, 649–652 (2006).

    CAS  PubMed  Google Scholar 

  74. 74.

    Todd, J. D., Curson, A. R. J., Dupont, C. L., Nicholson, P. & Johnston, A. W. B. The dddP gene, encoding a novel enzyme that converts dimethylsulfoniopropionate into dimethyl sulfide, is widespread in ocean metagenomes and marine bacteria and also occurs in some Ascomycete fungi. Environ. Microbiol. 11, 1376–1385 (2009).

    CAS  PubMed  Google Scholar 

  75. 75.

    Xie, J. B. et al. Comparative genomic analysis of N2-fixing and non-N2-fixing Paenibacillus spp.: organization, evolution and expression of the nitrogen fixation genes. PLoS Genet. 10, e1004231 (2014).

    PubMed  PubMed Central  Google Scholar 

  76. 76.

    Gaby, J. C. & Buckley, D. H. A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen-fixing bacteria. Database 2014, bau001 (2014).

    PubMed  PubMed Central  Google Scholar 

  77. 77.

    Mehta, M. P., Butterfield, D. A. & Baross, J. A. Phylogenetic diversity of nitrogenase (nifH) genes in deep-sea and hydrothermal vent environments of the Juan de Fuca Ridge. Appl. Environ. Microbiol. 69, 960–970 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    EDDY, S. R. A new generation of homology search tools based on probabilistic inference. Genome Inform. 23, 205–211 (2009).

    PubMed  Google Scholar 

  79. 79.

    Kolde, R. pheatmap: pretty heatmaps. R package version 61 (2012).

  80. 80.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013).

  81. 81.

    McMillan, J., Yellowlees, D., Heyward, A., Harrison, P. & Miller, D. J. Preparation of high molecular weight DNA from hermatypic corals and its use for DNA hybridization and cloning. Mar. Biol. 98, 271–276 (1988).

    CAS  Google Scholar 

  82. 82.

    Huang, S. et al. HaploMerger: reconstructing allelic relationships for polymorphic diploid genome assemblies. Genome Res. 22, 1581–1588 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Luo, R. et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1, 18 (2012).

    PubMed  PubMed Central  Google Scholar 

  84. 84.

    Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).

    CAS  PubMed  Google Scholar 

  85. 85.

    Li, W. & Godzik, A. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

    CAS  PubMed  Google Scholar 

  86. 86.

    Boeckmann, B. et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 31, 365–370 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Remmert, M., Biegert, A., Hauser, A. & Söding, J. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat. Methods 9, 173–175 (2012).

    CAS  Google Scholar 

  88. 88.

    Stanke, M. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, 435–439 (2006).

    Google Scholar 

  89. 89.

    Korf, I. Gene finding in novel genomes. BMC Bioinform. 5, 59 (2004).

    Google Scholar 

  90. 90.

    Borodovsky, M. & Lomsadze, A. Eukaryotic gene prediction using GeneMark.hmm-E and GeneMark-ES. Curr. Protoc. Bioinform. 4, 1–11 (2011).

    Google Scholar 

  91. 91.

    Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879 (2004).

    CAS  PubMed  Google Scholar 

  92. 92.

    Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, R7 (2008).

    PubMed  PubMed Central  Google Scholar 

  93. 93.

    O’Brien, K. P., Remm, M. & Sonnhammer, E. L. L. Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res. 33, 476–480 (2005).

    Google Scholar 

  94. 94.

    Liu, H. et al. Symbiodinium genomes reveal adaptive evolution of functions related to coral-dinoflagellate symbiosis. Commun. Biol. 1, 95 (2018).

    PubMed  PubMed Central  Google Scholar 

  95. 95.

    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. 97.

    Lin, S. et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350, 691–694 (2015).

    CAS  PubMed  Google Scholar 

  98. 98.

    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. 99.

    Xue, W. et al. L_RNA_scaffolder: scaffolding genomes with transcripts. BMC Genom. 14, 604 (2013).

    Google Scholar 

  100. 100.

    Haas, B. J. et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654–5666 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. 101.

    Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinform. 12, 491 (2011).

    Google Scholar 

  102. 102.

    Parra, G., Bradnam, K. & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061–1067 (2007).

    CAS  PubMed  Google Scholar 

  103. 103.

    Baumgarten, S. et al. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proc. Natl Acad. Sci. USA 112, 11893–11898 (2015).

    CAS  PubMed  Google Scholar 

  104. 104.

    Putnam, N. H. et al. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86–94 (2007).

    CAS  PubMed  Google Scholar 

  105. 105.

    Shoguchi, E. et al. Draft assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr. Biol. 23, 1399–1408 (2013).

    CAS  PubMed  Google Scholar 

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We dedicate this effort to the memory of S. Forêt who tragically passed away on the 17th of December 2016: S. Forêt was central to this consortium, an inspiration to us all for his humour, insight, knowledge and character. He unfortunately will not see the outcomes of this work but without him we would never have come so far. A dear friend has been taken too early but his legacy will continue. The data generated for this paper were funded by the Great Barrier Reef Foundation’s Resilient Coral Reefs Successfully Adapting to Climate Change program in collaboration with the Australian Government and Bioplatforms Australia through the Australian Government’s National Collaborative Research Infrastructure Strategy, Rio Tinto and a family foundation. The Reef Futures Genomics Consortium was established by the Great Barrier Reef Foundation to generate new perspectives, approaches and collaborations to fast-track the progress of reef management-relevant genomics-based coral reef climate adaptation research. G.W.T. is supported by an ARC Queen Elizabeth II Fellowship (DP1093175) and an Australian Research Council Future Fellowship FT170100070. S.R. is supported by funds from the ReFuGe2020 Consortium and from an ARC Discovery Project (DP160103811). C.X.C. and M.A.R. were supported by an Australian Research Council grant (DP150101875). C.R.V. was supported by funding from King Abdullah University of Science and Technology. D.J.M. was supported by funding from the ARC Centre of Excellence for Coral Reef Studies. S.F. was supported by the Australian Research Council grant CE140100020. We thank J. B. Raina, J. Boyd, B. Woodcroft, B. Kemish, S. Low, I. Krippner and M. Butler for helpful discussions and infrastructure support, and H. Smith for graphical design of the coral metabolism schematic.

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S.J.R., C.X.C., H.Y., M.A.R., D.J.M., C.R.V., S.F., G.W.T. and D.G.B. designed the overall study and procured funding with help from the ReFuGe2020 Consortium. D.G.B. and S.F. coordinated sampling efforts and K.M.M., S.F. and S.C.B. collected and processed the samples. S.J.R., C.M.S., A.B., L.F.M., A.U.G., C.R.V., G.W.T. and D.G.B. conducted the main bioinformatics analysis of the bacterial and archaeal genomes; H.Y., S.F. and D.J.M. focused on the coral-related data, and C.X.C., S.F., and M.A.R. focused on analysis of Cladocopium C15. S.J.R., C.M.S., L.F.M., G.W.T. and D.G.B. wrote the manuscript with contributions from C.R.V. All authors reviewed and approved the final manuscript.

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Correspondence to Gene W. Tyson.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–7, Supplementary Notes and Supplementary Table titles.

Reporting Summary

Supplementary Table 1

Taxonomy and genome statistics for all 52 P. lutea and 57 seawater MAGs.

Supplementary Table 2

Table of Pfams enriched in P. lutea-associated MAGs versus MAGs from GBR seawater.

Supplementary Table 3

Table of Pfams enriched in P. lutea-associated MAGs versus a set of representative seawater genomes from the Tara Oceans Metagenomic Survey.

Supplementary Table 4

Table of KEGG modules enriched in P. lutea-associated MAGs versus MAGs from GBR seawater.

Supplementary Table 5

Table of KEGG modules enriched in P. lutea-associated MAGs versus the Tara Oceans genomes.

Supplementary Table 6

List of gene annotations for Cladocopium C15.

Supplementary Table 7

List of nitrate transporters in Cladocopium C15.

Supplementary Table 8

Cladocopium C15 paired-end and mate-pair data statistics.

Supplementary Table 9

Number of reads in each assembly step for deriving the Cladocopium C15 genome.

Supplementary File 1

dddP gene sequences for Supplementary Fig. 4a.

Supplementary File 2

dmdA gene sequences for Supplementary Fig. 4b.

Supplementary File 7

nifH protein sequences from the metagenomic reads.

Supplementary File 9

Proteins sequences from nxrA and nxrB from Nitrospirota MAG Plut_88904.

Supplementary File 5

dddP GraftM output table.

Supplementary File 6

dmdA GraftM output table.

Supplementary File 8

nifH GraftM output table from the metagenomic reads.

Supplementary File 12

EnrichM KEGG annotation matrix.

Supplementary File 13

EnrichM Pfam annotation matrix.

Supplementary File 3

dddP tree file.

Supplementary File 4

dmdA tree file.

Supplementary File 10

nxrA GraftM output table.

Supplementary File 11

nxrB GraftM output table.

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Robbins, S.J., Singleton, C.M., Chan, C.X. et al. A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat Microbiol 4, 2090–2100 (2019). https://doi.org/10.1038/s41564-019-0532-4

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