N-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host
Abstract The clownfish - sea anemone system is a great example of symbiotic mutualism where host «toxicity» does not impact its symbiont partner, although the underlying protection mechanism remains unclear. The regulation of nematocyst discharge in cnidarians involves N-acetylated sugars like siali...
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Nature Portfolio
2025-01-01
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| author | Sara Heim Tony Teav Fabio Cortesi Hector Gallart-Ayala Julijana Ivanisevic Nicolas Salamin |
| author_facet | Sara Heim Tony Teav Fabio Cortesi Hector Gallart-Ayala Julijana Ivanisevic Nicolas Salamin |
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| description | Abstract The clownfish - sea anemone system is a great example of symbiotic mutualism where host «toxicity» does not impact its symbiont partner, although the underlying protection mechanism remains unclear. The regulation of nematocyst discharge in cnidarians involves N-acetylated sugars like sialic acid, that bind chemoreceptors on the tentacles of sea anemones, leading to the release of stings. It has been suggested that clownfish could be deprived of sialic acid on their skin surface, sparing them from being stung and facilitating mutualism with sea anemones. In this study, we sampled the skin mucus of two anemone symbionts, the clownfish Amphiprion akindynos and the juvenile damselfish Dascyllus trimaculatus, as well as two non-symbiotic adult damselfish Pomacentrus moluccensis and P. pavo. The free and total sialic acid content, including its conjugated form, and three other intermediates of this pathway were quantified using a stable isotope dilution mass spectrometry approach. We found significantly higher levels of sialic acid and its precursor in the non-symbiotic damselfishes. Concentrations of total sialic acid in anemone symbionts ranged between 13 µM and 16 µM, whereas the non-symbiotic damselfishes ranged between 21 µM and 30 µM. The presence of this metabolite and its precursors, as triggers of nematocyst discharge, in anemone symbionts, suggests that this is not the direct mechanism of protection or that the trigger is concentration dependent. This experiment demonstrates that anemone symbionts are not spared by nematocysts because of a lack of N-acetylated sugars, as previously thought, rather the biochemical mechanisms involving N-acetylated sugars are more complex than just a presence/absence of these molecules. |
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| publishDate | 2025-01-01 |
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| spelling | doaj-art-69a8e27e9e6c4d1186d73d1da3d134982025-01-19T12:21:48ZengNature PortfolioScientific Reports2045-23222025-01-0115111210.1038/s41598-024-84495-wN-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone hostSara Heim0Tony Teav1Fabio Cortesi2Hector Gallart-Ayala3Julijana Ivanisevic4Nicolas Salamin5Department of Computational Biology, Faculty of Biology and Medicine, University of LausanneMetabolomics and Lipidomics Unit, Faculty of Biology and Medicine, University of LausanneSchool of the Environment and Queensland Brain Institute, University of QueenslandMetabolomics and Lipidomics Unit, Faculty of Biology and Medicine, University of LausanneMetabolomics and Lipidomics Unit, Faculty of Biology and Medicine, University of LausanneDepartment of Computational Biology, Faculty of Biology and Medicine, University of LausanneAbstract The clownfish - sea anemone system is a great example of symbiotic mutualism where host «toxicity» does not impact its symbiont partner, although the underlying protection mechanism remains unclear. The regulation of nematocyst discharge in cnidarians involves N-acetylated sugars like sialic acid, that bind chemoreceptors on the tentacles of sea anemones, leading to the release of stings. It has been suggested that clownfish could be deprived of sialic acid on their skin surface, sparing them from being stung and facilitating mutualism with sea anemones. In this study, we sampled the skin mucus of two anemone symbionts, the clownfish Amphiprion akindynos and the juvenile damselfish Dascyllus trimaculatus, as well as two non-symbiotic adult damselfish Pomacentrus moluccensis and P. pavo. The free and total sialic acid content, including its conjugated form, and three other intermediates of this pathway were quantified using a stable isotope dilution mass spectrometry approach. We found significantly higher levels of sialic acid and its precursor in the non-symbiotic damselfishes. Concentrations of total sialic acid in anemone symbionts ranged between 13 µM and 16 µM, whereas the non-symbiotic damselfishes ranged between 21 µM and 30 µM. The presence of this metabolite and its precursors, as triggers of nematocyst discharge, in anemone symbionts, suggests that this is not the direct mechanism of protection or that the trigger is concentration dependent. This experiment demonstrates that anemone symbionts are not spared by nematocysts because of a lack of N-acetylated sugars, as previously thought, rather the biochemical mechanisms involving N-acetylated sugars are more complex than just a presence/absence of these molecules.https://doi.org/10.1038/s41598-024-84495-wClownfishDamselfishMucusN-acetylated-sugarsMutualismMetabolomics |
| spellingShingle | Sara Heim Tony Teav Fabio Cortesi Hector Gallart-Ayala Julijana Ivanisevic Nicolas Salamin N-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host Scientific Reports Clownfish Damselfish Mucus N-acetylated-sugars Mutualism Metabolomics |
| title | N-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host |
| title_full | N-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host |
| title_fullStr | N-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host |
| title_full_unstemmed | N-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host |
| title_short | N-acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host |
| title_sort | n acetylated sugars in clownfish and damselfish skin mucus as messengers involved in chemical recognition by anemone host |
| topic | Clownfish Damselfish Mucus N-acetylated-sugars Mutualism Metabolomics |
| url | https://doi.org/10.1038/s41598-024-84495-w |
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