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Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family2.34 MB
Published VersionCC BY V4.0, Open Access
Journal article
Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family
BMC Biology, Vol.21, pp.1-25
2023
PMID: 37226201
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.
Details
- Title
- Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family
- Authors
- Lauren M Ashwood (Corresponding Author) - Queensland University of TechnologyKhaled A Elnahriry - Monash UniversityZachary K Stewart - Queensland University of TechnologyThomas Shafee - La Trobe UniversityMuhammad Umair Naseem - University of DebrecenTibor G Szanto - University of DebrecenChloé A van der Burg - Queensland University of TechnologyHayden L Smith - Queensland University of TechnologyJoachim M Surm - Hebrew University of JerusalemEivind A B Undheim - University of OsloBruno Madio - The University of QueenslandBrett R Hamilton - The University of QueenslandShaodong Guo - The University of QueenslandDorothy C C Wai - Monash UniversityVictoria L Coyne - Queensland University of TechnologyMatthew J Phillips - Queensland University of TechnologyKevin J Dudley - Queensland University of TechnologyDavid A Hurwood - Queensland University of TechnologyGyorgy Panyi - University of DebrecenGlenn F King - The University of QueenslandAna Pavasovic - Queensland University of TechnologyRaymond S Norton - Monash UniversityPeter J Prentis - Queensland University of Technology
- Publication details
- BMC Biology, Vol.21, pp.1-25
- Publisher
- BioMed Central Ltd.
- Date published
- 2023
- DOI
- 10.1186/s12915-023-01617-y
- ISSN
- 1741-7007
- PMID
- 37226201
- Copyright note
- © The Author(s) 2023. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
- Data Availability
- All data generated or analysed during this study are included in this published article, its supplementary information files, and publicly available repositories. Raw RNA reads for T. stephensoni and A. tenebrosa are available at the NCBI Sequence Read Archive (SRA) under BioProjects PRJNA728752 [58, 146], PRJNA350366 [33, 147] and PRJNA313244 [104, 148]. Accession numbers for each tissue sample are given in Additional file 15: Table S4. Assembled genomes for T. stephensoni and A. tenebrosa have been uploaded to NCBI GenBank under accession numbers JALIZF000000000 [149] and JALIZE000000000 [150], respectively. The MS proteomics data have been uploaded to the ProteomeXchange Consortium via the PRIDE [151] partner repository with the dataset identifier PXD029717 [58, 152]. Custom pipelines and scripts can be accessed through the zkstewart GitHub repository [79,80,81, 86, 103, 120, 129, 132]. Genome annotations and alignment files used in this study have also been uploaded as GFF3 and FASTA files to figshare (https://doi.org/10.6084/m9.figshare.22777052).
- Organisation Unit
- School of Science, Technology and Engineering
- Language
- English
- Record Identifier
- 991054498002621
- Output Type
- Journal article
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