Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family
Abstract Background The ShK toxin from Stichodactyla helianthus has established the therapeutic potential of sea anemone venom peptides, but many lineage-specific toxin families in Actiniarians remain uncharacterised. One such peptide family, sea anemone 8 (SA8), is present in all five sea anemone s...
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BMC
2023-05-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01617-y |
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| author | Lauren M. Ashwood Khaled A. Elnahriry Zachary K. Stewart Thomas Shafee Muhammad Umair Naseem Tibor G. Szanto Chloé A. van der Burg Hayden L. Smith Joachim M. Surm Eivind A. B. Undheim Bruno Madio Brett R. Hamilton Shaodong Guo Dorothy C. C. Wai Victoria L. Coyne Matthew J. Phillips Kevin J. Dudley David A. Hurwood Gyorgy Panyi Glenn F. King Ana Pavasovic Raymond S. Norton Peter J. Prentis |
| author_facet | Lauren M. Ashwood Khaled A. Elnahriry Zachary K. Stewart Thomas Shafee Muhammad Umair Naseem Tibor G. Szanto Chloé A. van der Burg Hayden L. Smith Joachim M. Surm Eivind A. B. Undheim Bruno Madio Brett R. Hamilton Shaodong Guo Dorothy C. C. Wai Victoria L. Coyne Matthew J. Phillips Kevin J. Dudley David A. Hurwood Gyorgy Panyi Glenn F. King Ana Pavasovic Raymond S. Norton Peter J. Prentis |
| author_sort | Lauren M. Ashwood |
| collection | DOAJ |
| description | Abstract Background The ShK toxin from Stichodactyla helianthus has established the therapeutic potential of sea anemone venom peptides, but many lineage-specific toxin families in Actiniarians remain uncharacterised. One such peptide family, sea anemone 8 (SA8), is present in all five sea anemone superfamilies. We explored the genomic arrangement and evolution of the SA8 gene family in Actinia tenebrosa and Telmatactis stephensoni, characterised the expression patterns of SA8 sequences, and examined the structure and function of SA8 from the venom of T. stephensoni. Results We identified ten SA8-family genes in two clusters and six SA8-family genes in five clusters for T. stephensoni and A. tenebrosa, respectively. Nine SA8 T. stephensoni genes were found in a single cluster, and an SA8 peptide encoded by an inverted SA8 gene from this cluster was recruited to venom. We show that SA8 genes in both species are expressed in a tissue-specific manner and the inverted SA8 gene has a unique tissue distribution. While the functional activity of the SA8 putative toxin encoded by the inverted gene was inconclusive, its tissue localisation is similar to toxins used for predator deterrence. We demonstrate that, although mature SA8 putative toxins have similar cysteine spacing to ShK, SA8 peptides are distinct from ShK peptides based on structure and disulfide connectivity. Conclusions Our results provide the first demonstration that SA8 is a unique gene family in Actiniarians, evolving through a variety of structural changes including tandem and proximal gene duplication and an inversion event that together allowed SA8 to be recruited into the venom of T. stephensoni. |
| first_indexed | 2024-03-13T08:58:06Z |
| format | Article |
| id | doaj.art-21a4debffec04564ae9a29b4a8776746 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-03-13T08:58:06Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-21a4debffec04564ae9a29b4a87767462023-05-28T11:27:40ZengBMCBMC Biology1741-70072023-05-0121112510.1186/s12915-023-01617-yGenomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin familyLauren M. Ashwood0Khaled A. Elnahriry1Zachary K. Stewart2Thomas Shafee3Muhammad Umair Naseem4Tibor G. Szanto5Chloé A. van der Burg6Hayden L. Smith7Joachim M. Surm8Eivind A. B. Undheim9Bruno Madio10Brett R. Hamilton11Shaodong Guo12Dorothy C. C. Wai13Victoria L. Coyne14Matthew J. Phillips15Kevin J. Dudley16David A. Hurwood17Gyorgy Panyi18Glenn F. King19Ana Pavasovic20Raymond S. Norton21Peter J. Prentis22School of Biology and Environmental Science, Faculty of Science, Queensland University of TechnologyMedicinal Chemistry, Monash Institute of Pharmaceutical Sciences, Monash UniversityCentre for Agriculture and the Bioeconomy, Queensland University of TechnologyDepartment of Animal Plant & Soil Sciences, La Trobe UniversityDepartment of Biophysics and Cell Biology, Faculty of Medicine, University of DebrecenDepartment of Biophysics and Cell Biology, Faculty of Medicine, University of DebrecenSchool of Biology and Environmental Science, Faculty of Science, Queensland University of TechnologySchool of Biology and Environmental Science, Faculty of Science, Queensland University of TechnologyDepartment of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of JerusalemDepartment of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of OsloInstitute for Molecular Bioscience, The University of QueenslandCentre for Advanced Imaging, The University of QueenslandInstitute for Molecular Bioscience, The University of QueenslandMedicinal Chemistry, Monash Institute of Pharmaceutical Sciences, Monash UniversityResearch Infrastructure, Central Analytical Research Facility, Queensland University of TechnologySchool of Biology and Environmental Science, Faculty of Science, Queensland University of TechnologySchool of Biology and Environmental Science, Faculty of Science, Queensland University of TechnologySchool of Biology and Environmental Science, Faculty of Science, Queensland University of TechnologyDepartment of Biophysics and Cell Biology, Faculty of Medicine, University of DebrecenInstitute for Molecular Bioscience, The University of QueenslandSchool of Biomedical Sciences, Faculty of Health, Queensland University of TechnologyMedicinal Chemistry, Monash Institute of Pharmaceutical Sciences, Monash UniversitySchool of Biology and Environmental Science, Faculty of Science, Queensland University of TechnologyAbstract Background The ShK toxin from Stichodactyla helianthus has established the therapeutic potential of sea anemone venom peptides, but many lineage-specific toxin families in Actiniarians remain uncharacterised. One such peptide family, sea anemone 8 (SA8), is present in all five sea anemone superfamilies. We explored the genomic arrangement and evolution of the SA8 gene family in Actinia tenebrosa and Telmatactis stephensoni, characterised the expression patterns of SA8 sequences, and examined the structure and function of SA8 from the venom of T. stephensoni. Results We identified ten SA8-family genes in two clusters and six SA8-family genes in five clusters for T. stephensoni and A. tenebrosa, respectively. Nine SA8 T. stephensoni genes were found in a single cluster, and an SA8 peptide encoded by an inverted SA8 gene from this cluster was recruited to venom. We show that SA8 genes in both species are expressed in a tissue-specific manner and the inverted SA8 gene has a unique tissue distribution. While the functional activity of the SA8 putative toxin encoded by the inverted gene was inconclusive, its tissue localisation is similar to toxins used for predator deterrence. We demonstrate that, although mature SA8 putative toxins have similar cysteine spacing to ShK, SA8 peptides are distinct from ShK peptides based on structure and disulfide connectivity. Conclusions Our results provide the first demonstration that SA8 is a unique gene family in Actiniarians, evolving through a variety of structural changes including tandem and proximal gene duplication and an inversion event that together allowed SA8 to be recruited into the venom of T. stephensoni.https://doi.org/10.1186/s12915-023-01617-ySea anemoneToxin evolutionGenomeNeofunctionalizationPeptide synthesisDisulfide connectivity |
| spellingShingle | Lauren M. Ashwood Khaled A. Elnahriry Zachary K. Stewart Thomas Shafee Muhammad Umair Naseem Tibor G. Szanto Chloé A. van der Burg Hayden L. Smith Joachim M. Surm Eivind A. B. Undheim Bruno Madio Brett R. Hamilton Shaodong Guo Dorothy C. C. Wai Victoria L. Coyne Matthew J. Phillips Kevin J. Dudley David A. Hurwood Gyorgy Panyi Glenn F. King Ana Pavasovic Raymond S. Norton Peter J. Prentis Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family BMC Biology Sea anemone Toxin evolution Genome Neofunctionalization Peptide synthesis Disulfide connectivity |
| title | Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family |
| title_full | Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family |
| title_fullStr | Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family |
| title_full_unstemmed | Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family |
| title_short | Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family |
| title_sort | genomic functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family |
| topic | Sea anemone Toxin evolution Genome Neofunctionalization Peptide synthesis Disulfide connectivity |
| url | https://doi.org/10.1186/s12915-023-01617-y |
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