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

Nature Microbiology volume 4, pages 2090–2100 (2019)Cite this article

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Abstract

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.

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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.

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Acknowledgements

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.

Author information

Author notes

  1. A full list of authors and their affiliations appears at the end of the paper.

Authors and Affiliations

  1. Australian Centre for Ecogenomics, The University of Queensland, Brisbane, Queensland, Australia

    Steven J. Robbins, Caitlin M. Singleton, Lauren F. Messer, Aileen U. Geers, Alexander Baker, Francesco Rubino, Steven J. Robbins, Caitlin M. Singleton, Lauren F. Messer, Aileen U. Geers, Alexander Baker, Gene W. Tyson & Gene W. Tyson

  2. Institute for Molecular Bioscience, The University of Queensland, Brisbane, Queensland, Australia

    Cheong Xin Chan, Mark A. Ragan, Cheong Xin Chan & Mark A. Ragan

  3. School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland, Australia

    Cheong Xin Chan & Cheong Xin Chan

  4. Division of Ecology & Evolution, Research School of Biology, Australian National University, Canberra, Australia

    Hua Ying, Sylvain Forêt, Eldon Ball, Hua Ying & Sylvain Foret

  5. Australian Institute of Marine Science, Townsville, Queensland, Australia

    Sara C. Bell, Kathleen M. Morrow, Karen Weynberg, Sara C. Bell, Kathleen M. Morrow, David G. Bourne & David G. Bourne

  6. Department of Environmental Science and Policy, George Mason University, Fairfax, VA, USA

    Kathleen M. Morrow & Kathleen M. Morrow

  7. Department of Cellular, Molecular, and Biomedical Sciences, University of New Hampshire, Durham, NH, USA

    Kathleen M. Morrow & Kathleen M. Morrow

  8. ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia

    David J. Miller, Bill Leggat, Susan Sprungala & David J. Miller

  9. Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia

    Michael Berumen, Manuel Aranda, Timothy Ravasi, Christian R. Voolstra & Christian R. Voolstra

  10. Department of Biology, University of Konstanz, Konstanz, Germany

    Christian R. Voolstra & Christian R. Voolstra

  11. College of Science and Engineering, James Cook University, Townsville, Queensland, Australia

    David G. Bourne & David G. Bourne

  12. Great Barrier Reef Marine Park Authority, Townsville, Queensland, Australia

    Roger Beeden

  13. Global Change Institute, The University of Queensland, Brisbane, Queensland, Australia

    Pim Bongaerts & Ove Hoegh-Guldberg

  14. Department of Molecular and Cell Biology, James Cook University, Townsville, Queensland, Australia

    Ira Cooke

  15. Bioplatforms, Sydney, New South Wales, Australia

    Anna Fitzgerald & Catherine Shang

  16. Great Barrier Reef Foundation, Brisbane, Queensland, Australia

    Petra Lundgren & Theresa Fyffe

  17. School of BioSciences, University of Melbourne, Melbourne, Victoria, Australia

    Madeleine van Oppen

  18. Australian Institute of Marine Science, Townsville, Queensland, Australia

    Madeleine van Oppen

Authors
  1. Steven J. Robbins
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  2. Caitlin M. Singleton
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  3. Cheong Xin Chan
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Consortia

ReFuGe2020 Consortium

  • Eldon Ball
  • , Roger Beeden
  • , Michael Berumen
  • , Manuel Aranda
  • , Timothy Ravasi
  • , Pim Bongaerts
  • , Ove Hoegh-Guldberg
  • , Ira Cooke
  • , Bill Leggat
  • , Susan Sprungala
  • , Anna Fitzgerald
  • , Catherine Shang
  • , Petra Lundgren
  • , Theresa Fyffe
  • , Francesco Rubino
  • , Madeleine van Oppen
  • , Karen Weynberg
  • , Steven J. Robbins
  • , Caitlin M. Singleton
  • , Cheong Xin Chan
  • , Lauren F. Messer
  • , Aileen U. Geers
  • , Hua Ying
  • , Alexander Baker
  • , Sara C. Bell
  • , Kathleen M. Morrow
  • , Mark A. Ragan
  • , David J. Miller
  • , Sylvain Foret
  • , Christian R. Voolstra
  • , Gene W. Tyson
  •  & David G. Bourne

Contributions

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.

Corresponding author

Correspondence to Gene W. Tyson.

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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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