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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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).
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.
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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.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Figs. 1–7, Supplementary Notes and Supplementary Table titles.
Taxonomy and genome statistics for all 52 P. lutea and 57 seawater MAGs.
Table of Pfams enriched in P. lutea-associated MAGs versus MAGs from GBR seawater.
Table of Pfams enriched in P. lutea-associated MAGs versus a set of representative seawater genomes from the Tara Oceans Metagenomic Survey.
Table of KEGG modules enriched in P. lutea-associated MAGs versus MAGs from GBR seawater.
Table of KEGG modules enriched in P. lutea-associated MAGs versus the Tara Oceans genomes.
List of gene annotations for Cladocopium C15.
List of nitrate transporters in Cladocopium C15.
Cladocopium C15 paired-end and mate-pair data statistics.
Number of reads in each assembly step for deriving the Cladocopium C15 genome.
dddP gene sequences for Supplementary Fig. 4a.
dmdA gene sequences for Supplementary Fig. 4b.
nifH protein sequences from the metagenomic reads.
Proteins sequences from nxrA and nxrB from Nitrospirota MAG Plut_88904.
dddP GraftM output table.
dmdA GraftM output table.
nifH GraftM output table from the metagenomic reads.
EnrichM KEGG annotation matrix.
EnrichM Pfam annotation matrix.
dddP tree file.
dmdA tree file.
nxrA GraftM output table.
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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