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Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment

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Abstract

Climate change threatens the survival of scleractinian coral from exposure to concurrent ocean warming, acidification and deoxygenation; how corals can potentially adapt to this trio of stressors is currently unknown. This study investigates three coral species (Acropora muricata, Acropora pulchra and Porites lutea) dominant in an extreme mangrove lagoon (Bouraké, New Caledonia) where abiotic conditions exceed those predicted for many reef sites over the next 100 years under climate change and compared them to conspecifics from an environmentally more benign reef habitat. We studied holobiont physiology as well as plasticity in coral-associated microorganisms (Symbiodiniaceae and bacteria) through ITS2 and 16S rRNA sequencing, respectively. We hypothesised that differences in coral-associated microorganisms (Symbiodiniaceae and bacteria) between the lagoonal and adjacent reef habitats may support coral host productivity and ultimately the ability of corals to live in extreme environments. In the lagoon, all coral species exhibited  a metabolic adjustment of reduced photosynthesis-to-respiration ratios (P/R), but this was accompanied by highly divergent coral host-specific microbial associations. This was substantiated by the absence of shared ITS2-type profiles (proxies for Symbiodiniaceae genotypes). We observed that ITS2 profiles originating from Durusdinium taxa made up < 3% and a novel Symbiodinium ITS2 profile A1-A1v associated with A. pulchra. Bacterial community profiles were also highly divergent in  corals from the lagoonal environment, whereas corals from the reef site were consistently dominated by Hahellaceae, Endozoicomonas. As such, differences in host–microorganism associations aligned with different physiologies and habitats. Our results argue that a multitude of host–microorganism associations are required to fulfill the changing nutritional demands of corals persisting into environments that parallel climate change scenarios.

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Availability of data and materials

All data generated or analysed during this study are included in this published article [and its supplementary information files]. All raw sequence data are accessible under NCBI’s BioProject (ID ITS2: PRJNA510616 https://www.ncbi.nlm.nih.gov/bioproject/PRJNA510616, 16S rRNA: PRJNA510614 https://www.ncbi.nlm.nih.gov/bioproject/PRJNA510614).

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Acknowledgements

We wish to express our deepest thanks to C. Payri and the captains of the IRD vessels for their fieldwork assistance. We also thank B. Pelletier and the Grand Observatoire du Pacifique du Sud (GOPS), for use of their instruments and facilities, and F. Benzoni for verifying our coral taxonomic identification.

Funding

EFC was supported by an Endeavour Postdoctoral Fellowship to collect and process the data. The contribution of DJS and EFC to manuscript writing and final preparation was through an Australian Research Council Discovery Project (160100271 to D.JS). BCCH, CP and CRV acknowledge funding by the King Abdullah University of Science and Technology (KAUST) and would like to thank the Bioscience Core Lab (BCL) at KAUST for sequencing assistance. We also wish to thank to Fonds Pacifique for financial support (Project 1722 ‘Identifying the value of New Caledonia’s “extreme” corals to manage reefs under climate change’ to DJS, RRM, EFC) in funding the workshop COLIMATIC where data for this manuscript were first discussed.

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Authors and Affiliations

  1. Climate Change Cluster, University of Technology Sydney, Ultimo, NSW, 2007, Australia

    Emma F. Camp, David J. Suggett, Matthew R. Nitschke & Stephanie G. Gardner

  2. Red Sea Research Center, Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900, Saudi Arabia

    Claudia Pogoreutz, Benjamin C. C. Hume & Christian R. Voolstra

  3. Department of Biology and Center for Environmental and Marine Studies, University of Aveiro, 3810-193, Aveiro, Portugal

    Matthew R. Nitschke

  4. Laboratoire d’Excellence «CORAIL», Institut de Recherche pour le Développement, Centre IRD de Nouméa, ENTROPIE (UMR250), BP A5, 98848, Nouméa Cedex, New Caledonia

    Fanny Houlbreque, Marco Zampighi & Riccardo Rodolfo-Metalpa

  5. Centre for Marine Science and Innovation, School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW, 2052, Australia

    Stephanie G. Gardner

  6. Department of Biology, University of Konstanz, Konstanz, 78457, Germany

    Claudia Pogoreutz & Christian R. Voolstra

Authors
  1. Emma F. Camp
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  2. David J. Suggett
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  3. Claudia Pogoreutz
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  4. Matthew R. Nitschke
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  7. Stephanie G. Gardner
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  10. Christian R. Voolstra
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Contributions

EFC, DJS, FH and RRM led the project planning. EFC and DJS designed the study. EFC, DJS, MRN, MZ, RRM and SGG contributed to data collection. EFC undertook the DNA extractions with CRV carrying out the sequencing. CP, BCCH, EFC, MRN and CRV conducted the data analysis. MRN, EFC and BCCH compiled the figures. EFC, DJS and CRV led the writing of the manuscript with all authors contributing to the final manuscript preparation.

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Correspondence to Emma F. Camp.

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Camp, E.F., Suggett, D.J., Pogoreutz, C. et al. Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment. Coral Reefs 39, 701–716 (2020). https://doi.org/10.1007/s00338-019-01889-3

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