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Symbiotic plasticity of Symbiodinium in a common excavating sponge

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Abstract

Dinoflagellates of the genus Symbiodinium are symbiotic with a wide range of marine invertebrates. Broadly described as a mutualistic symbiosis, possible parasitic tendencies of Symbiodinium are less well known. The present study investigated the potential for mutualistic Symbiodinium to become parasitic in the excavating sponge Cliona orientalis, a ubiquitous bioeroder on Indo-Pacific coral reefs. We report the surprising observation that the growth, asexual reproduction and population density of Symbiodinium in C. orientalis were apparently unaffected when photosynthesis was reduced to zero in complete darkness for 20 days. Symbiodinium remained functional in hospite following the dark treatment, although with reduced photosynthetic efficiency compared to the control treatment under a daily light cycle. Rates of dark respiration and net uptake of heterotrophic carbon by the holobiont were similar between the control and dark treatments. However, dark-treated C. orientalis displayed a negative carbon budget that indicated compromised host growth, along with reduced biomass and bioerosion capability. Our findings suggest that, when lacking photo-autotrophic energy, Symbiodinium possibly sustains itself through heterotrophy at the expense of its hosts. This transfer of host materials to the symbiont suggests parasitism that may be associated with the observed deterioration of C. orientalis in the dark treatment. Overall, our study implies plasticity of Symbiodinium in terms of shifting its symbiotic role between mutualism and parasitism.

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Acknowledgements

We acknowledge Moreton Bay Research Station of The University of Queensland, and E Lewis, N Van Dyck, K Townsend, WKW Loh, G Bernal Carrillo and A Chai for their assistance in the field and the laboratory. We also thank MS Hill and the three anonymous reviewers who provided valuable comments on this article.

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  1. James K. H. Fang

    Present address: Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong

Authors and Affiliations

  1. Coral Reef Ecosystems Laboratory, School of Biological Sciences, The University of Queensland, St. Lucia, QLD, 4072, Australia

    James K. H. Fang, Ove Hoegh-Guldberg & Sophie Dove

  2. Australian Research Council Centre of Excellence for Coral Reef Studies, The University of Queensland, St. Lucia, QLD, 4072, Australia

    James K. H. Fang, Ove Hoegh-Guldberg & Sophie Dove

  3. School of Earth and Environment and Oceans Institute, The University of Western Australia, Crawley, WA, 6009, Australia

    Christine H. L. Schönberg

  4. Global Change Institute, The University of Queensland, St. Lucia, QLD, 4072, Australia

    Ove Hoegh-Guldberg

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Correspondence to James K. H. Fang.

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This study was funded by the Australian Research Council (ARC) Linkage Grant LP0775303 (SD and OHG), and the ARC Centre of Excellence Grant CE0561435 (SD and OHG). None of the authors have a conflict of interest to declare. All sponge samples were collected under the permit QS2010/MAN79 provided by the Department of Environment and Resource Management, Australia. The use of Cliona orientalis in this study did not require an ethical approval.

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Fang, J.K.H., Schönberg, C.H.L., Hoegh-Guldberg, O. et al. Symbiotic plasticity of Symbiodinium in a common excavating sponge. Mar Biol 164, 104 (2017). https://doi.org/10.1007/s00227-017-3088-y

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