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Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta

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Abstract

Symbiosis between reef-building corals and unicellular algae (Symbiodiniaceae) fuels the growth and productivity of corals reefs. Capacity for Symbiodiniaceae to fix inorganic carbon (Ci) and translocate carbon compounds to the host is central to coral health, but how these processes change for corals thriving in environmental extremes remains largely unresolved. We investigate how a model coral—Pocillopora acuta—persists from a reef habitat into an adjacent extreme mangrove lagoon on the Great Barrier Reef. We combine respirometry and photophysiology measurements, Symbiodiniaceae genotyping, and 13C labelling to compare P. acuta metabolic performance across habitats, in relation to the Ci uptake and translocation capacity by symbionts’ autotrophy. We show that differences in P. acuta metabolic strategies across habitats align with a shift in dominant host-associated Symbiodiniaceae taxon, from Cladocopium in the reef to Durusdinium in the mangroves. This shift corresponded with a change in “photosynthetic strategy”, with P. acuta in the mangroves utilising absorbed light for photochemistry over non-photochemical quenching. Mangrove corals translocated similar proportions of carbon compared to the reefs, despite a lower Ci uptake. These trends indicate that coral survival in mangrove environments occurs through sustained translocation rate of organic compounds from coral symbionts to host.

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Acknowledgements

Contribution of D.J.S. was supported by an Australian Research Council Future Fellowship (FT130100202) and AMP Tomorrow Maker Award, and M.R., E.F.C. (data collection), and D.J.H. through ARC Discovery Grants (DP180100074 to D.J.S.). Additional contribution of E.F.C. to manuscript writing and final preparation was through the University of Technology Sydney Chancellor’s Postdoctoral Research Fellowship and ARC Discovery Early Career Research Award (DE190100142). The authors acknowledge the facilities and the scientific and technical assistance provided through the National Collaborative Research Infrastructure Strategy (NCRIS) by Microscopy Australia at the Australian Centre for Microscopy & Microanalysis at the University of Sydney and the Centre for Microscopy, Characterisation and Analysis (CMCA) at the University of Western Australia.

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Authors and Affiliations

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

    Mickael Ros, David J. Suggett, Trent Haydon, David J. Hughes, Mikael Kim, Mathieu Pernice, Jean-Baptiste Raina & Emma F. Camp

  2. Wavelength Reef Cruises, Port Douglas, QLD, 4877, Australia

    John Edmondson

  3. Centre for Microscopy, Characterisation and Analysis, University of Western Australia, Perth, WA, Australia

    Paul Guagliardo & Jeremy Bougoure

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  1. Mickael Ros
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Contributions

MR, DJS, EFC and JE designed and conducted all fieldwork and MR conducted experiments; MR and DJH designed the dual fractions incubation chambers, EFC performed respirometry measurements and symbiont identity analysis; DJS collected and analysed the photo-physiological data; MR, DJS, EFC collected the coral samples; MR, MP, EFC and JBR designed the stable isotope labelling experiments and MR performed incubations, cell density measurements, prepared samples for stable isotope analysis and analysed NanoSIMS images with the help of JBR; TH performed host and symbiont DNA extraction for identity analysis; MK, JBR and MP prepared the samples for NanoSIMS analysis; PG and JB performed the NanoSIMS image acquisition. MR, DJS, JBR and EFC wrote the manuscript; all authors provided subsequent editorials.

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Correspondence to Mickael Ros.

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Ros, M., Suggett, D.J., Edmondson, J. et al. Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta. Coral Reefs 40, 595–607 (2021). https://doi.org/10.1007/s00338-021-02066-1

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