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The influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis

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Abstract

We measured the relationship between symbiont diversity, nutritional potential, and symbiotic success in the cnidarian–dinoflagellate symbiosis, by infecting aposymbiotic (i.e. symbiont-free) specimens of the model sea anemone Aiptasia sp. with a range of Symbiodinium types. Four cultured heterologous Symbiodinium types (i.e. originally isolated from other host species) were used, plus both cultured and freshly isolated homologous zooxanthellae (i.e. from Aiptasia sp.). Rates of photosynthesis, respiration, and symbiont growth were measured during symbiosis establishment and used to estimate the contribution of the zooxanthellae to the animal’s respiratory carbon demands (CZAR). Anemones containing Symbiodinium B1 (both homologous and heterologous) tended to attain higher CZAR values and hence benefit most from their symbiotic partners. This was despite Symbiodinium B1 not achieving the highest cell densities, though it did grow more quickly during the earliest stages of the infection process. Rather, the heterologous Symbiodinium types A1.4, E2, and F5.1 attained the highest densities, with populations of E2 and F5.1 also exhibiting the highest photosynthetic rates. This apparent success was countered, however, by very high rates of symbiosis respiration that ultimately resulted in lower CZAR values. This study highlights the impact of symbiont type on the functionality and autotrophic potential of the symbiosis. Most interestingly, it suggests that certain heterologous symbionts may behave opportunistically, proliferating rapidly but in a manner that is energetically costly to the host. Such negative host–symbiont interactions may contribute to the host–symbiont specificity seen in cnidarian–dinoflagellate symbioses and potentially limit the potential for partner switching as an adaptive mechanism.

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Acknowledgments

We would like to thank Dr. C.B. Cook (Harbor Branch Oceanographic Institute, Florida Atlantic University, FL, USA), as well as two anonymous reviewers for their valuable comments on this manuscript. This work was supported by a Victoria University of Wellington postgraduate scholarship and faculty research grant awarded to DS.

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  1. Matthew R. Nitschke

    Present address: School of Biological Sciences, The University of Queensland, St Lucia, Brisbane, QLD, 4072, Australia

  2. Dorota E. Starzak

    Present address: School of Health Sciences, University of KwaZulu-Natal, University Rd, Westville, Durban, 4000, South Africa

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  1. School of Biological Sciences, Victoria University of Wellington, P.O. Box 600, Wellington, New Zealand

    Dorota E. Starzak, Matthew R. Nitschke & Simon K. Davy

  2. School of Biological Sciences, The University of Sydney, Sydney, NSW, 2006, Australia

    Rosanne G. Quinnell

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Starzak, D.E., Quinnell, R.G., Nitschke, M.R. et al. The influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis. Mar Biol 161, 711–724 (2014). https://doi.org/10.1007/s00227-013-2372-8

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