Better off alone? New insights in the symbiotic relationship between the flatworm Symsagittifera roscoffensis and the microalgae Tetraselmis convolutae

Abstract

The acoel flatworm Symsagittifera roscoffensis lives in obligatory symbiosis with the microalgal chlorophyte Tetraselmis convolutae. Although this interaction has been studied for more than a century, little is known on the potential reciprocal benefits of both partners, a subject that is still controversial. In order to provide new insights into this question, we have compared the photophysiology of the free-living microalgae to the symbiotic form in the flatworm, both acclimated at different light irradiances. Photosynthesis – Irradiance curves showed that the free-living T. convolutae had greater photosynthetic performance (i.e., oxygen production rates, ability to harvest light) than their symbiotic form, regardless of the light acclimation. However, they were affected by photoinhibition under high irradiances, which did not happen for the symbiotic form. The resistance of symbiotic microalgae to photoinhibition were corroborated by pigment analyses, which evidenced the induction of photoprotective mechanisms such as xanthophyll cycle as well as lutein and β-carotene accumulation. These processes were induced even under low light acclimation and exacerbated upon high light acclimation, suggesting a global stress situation for the symbiotic microalgae. We hypothesize that the internal conditions in the sub-epidermal zone of the flatworm (e.g., osmotic and pH), as well as the phototaxis toward high light imposed by the worm in its environment, would be major reasons for this chronic stress situation. Overall, our study suggests that the relationship between S. roscoffensis and T. convolutae may be a farming strategy in favor of the flatworm rather than a symbiosis with mutual benefits.

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Acknowledgments

This work was supported by the French program Investissement d’Avenir IDEALG. We thank the Roscoff Aquarium Services, especially Sébastien Henry and Ronan Garnier for their technical help and Xavier Bailly for his advices regarding Symsagittifera roscoffensis ecology and physiology (Research Federation 2424). We thank the Roscoff Culture Collection, in particular Ian Probert, for the isolation and maintenance and the Tetraselmis convoluta culture. We also thank Alexandra Michiels for help with R coding, and Francisco Rodriguez and José Luis Garrido for the interesting discussions on the HPLC results. Finally, we are grateful to the anonymous reviewer whose suggestions greatly improved the manuscript.

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Androuin, T., Six, C., Bordeyne, F. et al. Better off alone? New insights in the symbiotic relationship between the flatworm Symsagittifera roscoffensis and the microalgae Tetraselmis convolutae. Symbiosis (2020). https://doi.org/10.1007/s13199-020-00691-y

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Keywords

  • Symbiosis
  • Animal-plant
  • Photobiology
  • Symsagittifera roscoffensis
  • Tetraselmis convolutae