Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family

BMC Biology

Research Article

Brett R. Hamilton¹  Zachary K. Stewart²  Thomas Shafee³  Muhammad Umair Naseem⁴  Gyorgy Panyi⁴  Tibor G. Szanto⁴  Eivind A. B. Undheim⁵  Joachim M. Surm⁶  Shaodong Guo⁷  Bruno Madio⁷  Glenn F. King⁸  Dorothy C. C. Wai⁹  Khaled A. Elnahriry⁹  Raymond S. Norton^1,10  Victoria L. Coyne^1,11  Matthew J. Phillips^1,12  Hayden L. Smith^1,12  Lauren M. Ashwood^1,13  David A. Hurwood^1,14  Peter J. Prentis^1,14  Chloé A. van der Burg^1,15  Kevin J. Dudley^1,16  Ana Pavasovic^1,17 

[1] Centre for Advanced Imaging, The University of Queensland, 4072, St Lucia, QLD, Australia;Centre for Microscopy and Microanalysis, The University of Queensland, 4072, St Lucia, QLD, Australia;Centre for Agriculture and the Bioeconomy, Queensland University of Technology, 4000, Brisbane, QLD, Australia;Department of Animal Plant & Soil Sciences, La Trobe University, Melbourne, Australia;Swinburne University of Technology, Melbourne, VIC, Australia;Department of Biophysics and Cell Biology, Faculty of Medicine, University of Debrecen, 4032, Debrecen, Hungary;Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, PO Box 1066, Blindern, 0316, Oslo, Norway;Centre for Advanced Imaging, The University of Queensland, 4072, St Lucia, QLD, Australia;Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, 9190401, Jerusalem, Israel;Institute for Molecular Bioscience, The University of Queensland, 4072, St Lucia, QLD, Australia;Institute for Molecular Bioscience, The University of Queensland, 4072, St Lucia, QLD, Australia;ARC Centre for Innovations in Peptide and Protein Science, The University of Queensland, 4072, St Lucia, QLD, Australia;Medicinal Chemistry, Monash Institute of Pharmaceutical Sciences, Monash University, 3052, Parkville, VIC, Australia;Medicinal Chemistry, Monash Institute of Pharmaceutical Sciences, Monash University, 3052, Parkville, VIC, Australia;ARC Centre for Fragment-Based Design, Monash University, 3052, Parkville, VIC, Australia;Research Infrastructure, Central Analytical Research Facility, Queensland University of Technology, 4000, Brisbane, QLD, Australia;School of Biology and Environmental Science, Faculty of Science, Queensland University of Technology, 4000, Brisbane, QLD, Australia;School of Biology and Environmental Science, Faculty of Science, Queensland University of Technology, 4000, Brisbane, QLD, Australia;Cancer Program, QIMR Berghofer Medical Research Institute, 4006, Brisbane, QLD, Australia;School of Biology and Environmental Science, Faculty of Science, Queensland University of Technology, 4000, Brisbane, QLD, Australia;Centre for Agriculture and the Bioeconomy, Queensland University of Technology, 4000, Brisbane, QLD, Australia;School of Biology and Environmental Science, Faculty of Science, Queensland University of Technology, 4000, Brisbane, QLD, Australia;Department of Anatomy, School of Biomedical Sciences, University of Otago, 9016, Dunedin, New Zealand;School of Biology and Environmental Science, Faculty of Science, Queensland University of Technology, 4000, Brisbane, QLD, Australia;Research Infrastructure, Central Analytical Research Facility, Queensland University of Technology, 4000, Brisbane, QLD, Australia;School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, 4000, Brisbane, QLD, Australia;

关键词: Sea anemone;    Toxin evolution;    Genome;    Neofunctionalization;    Peptide synthesis;    Disulfide connectivity;   

DOI  :  10.1186/s12915-023-01617-y

 received in 2023-01-08, accepted in 2023-05-09,  发布年份 2023

来源: Springer

【 摘 要 】

BackgroundThe 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.ResultsWe 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.ConclusionsOur 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.

【 授权许可】

CC BY   
© The Author(s) 2023

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