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 freeliving 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.

Bisphenol A affects the development and the onset of photosymbiosis in the acoelSymsagittifera roscoffensis

“…This result is particularly concerning as this photosymbiotic acoel has an important ecological role. S. roscoffensis has a highly efficient photosynthetic ability and its large populations of the intertidal zone can generate a primary production close to those reported for coral reefs (Androuin et al, 2020; Thomas et al, 2023). Moreover, this species has been proposed as a possible natural bioremediator as it shows high nitrate assimilation rates, and it can thus act as an important in situ nitrate recycler in polluted marine environments (Carvalho et al, 2013).…”

Coordinated wound responses in a regenerative animal-algal holobiont

“…In the acoel, we found 14 transporters affected by Cl-runt knockdown. Two of these, Cl-slco4c1 and Cl-vha , were downregulated upon injury and could regulate the acidity of the extracellular environment 23 , 24 , 64 . A glutamate transporter, Cl-eaat1 , was also downregulated after injury and could affect the nitrogen cycling between the symbionts.…”

“…In free living algae, photosynthesis is modulated by multiple abiotic factors including light 16 , nutrients 17 , temperature 18 , and the availability of inorganic carbon 19 . In photosymbiosis, hosts can regulate the photosynthetic output of their endosymbiotic algae by modulating the concentrations of inorganic carbon and nitrogen 20 , 21 , adjusting the pH of the symbionts’ microenvironment 22 , 23 , and changing light intensity 24 . The study of regeneration in photosymbiotic animals, though rarely explored 25 , presents a great opportunity to unravel the molecular integration between host and symbionts.…”

Cladobranchia (Gastropoda, Nudibranchia) as a Promising Model to Understand the Molecular Evolution of Photosymbiosis in Animals

“…Future immuno-histochemical studies could give valuable insights into the localization of photosymbiosis-relevant receptors and their role in the nutritional exchange between the two partners, while metabolomics could provide important information on the interdependent nutrient exchange between both partners. Further, it remains to be shown whether in species with a stable photosymbiosis the symbiosis is beneficial for the host and whether the symbiosis is mutualistic or even some sort of parasitism as proposed for other photosymbiotic animals by some authors (Lesser et al, 2013;Blackstone and Golladay, 2018;Androuin et al, 2020).…”