Venoms for all occasions: the functional toxin profiles of different anatomical regions in sea anemones are related to their ecological function

Phylum Cnidaria is the oldest extant venomous group and is defined by the presence of nematocysts, specialised organelles responsible for venom production and delivery. While nematocysts and toxin peptides are distributed across the entire animal, nematocyst and venom profiles have been shown to differ across morphological structures in actiniarians. In this study, we explore the relationship between patterns of toxin expression and the ecological roles of discrete anatomical structures in Telmatactis stephensoni. Specifically, using a combination of proteomic and transcriptomic approaches, we examined whether there is a direct correlation between the functional similarity of regions and the similarity of their associated toxin expression profiles. We report that the regionalisation of toxin production is consistent with the partitioning of the ecological roles of venom across envenomating structures, and that three major functional regions are present in T. stephensoni— tentacles, epidermis and gastrodermis. Additionally, we find that structures which serve similar functions not only have comparable toxin profiles but also similar nematocyst types. There was no overlap in the toxins identified using proteomics and transcriptomics, however, the expression patterns of specific milked venom peptides were conserved across RNA-seq and mass spectrometry imaging datasets. Furthermore, based on our data, it appears that acontia of T. stephensoni may be transcriptionally inactive and only mature nematocyst are present in the distal portions of the threads. Overall, we find that the venom profile of different anatomical regions in sea anemones varies according to its ecological functions.

刺胞动物门（Cnidaria）是现存最古老的有毒类群，其鉴别特征为拥有刺细胞（nematocysts）——一类专司毒液产生与递送的特化细胞器。尽管刺细胞与毒素肽广泛分布于整个动物体，已有研究证实海葵类（actiniarians）的刺细胞与毒液谱会因形态结构的不同而存在差异。本研究以斯蒂芬森滨海葵（Telmatactis stephensoni）为研究对象，探究其毒素表达模式与离散解剖结构的生态功能之间的关联。具体而言，我们结合蛋白质组学（proteomics）与转录组学（transcriptomics）技术手段，验证了各解剖区域的功能相似性是否与其相关毒素表达谱的相似性存在直接相关性。本研究结果显示，毒素产生的区域化特征与毒液在不同毒液注入结构间的生态功能分化相一致，且斯蒂芬森滨海葵存在三大主要功能区域：触手、表皮与胃层（gastrodermis）。此外，我们发现功能相似的结构不仅具有相似的毒素谱，还拥有同类的刺细胞类型。不过，通过蛋白质组学与转录组学鉴定得到的毒素并无重叠，但特定挤取所得的毒液肽的表达模式在RNA-seq与质谱成像（mass spectrometry imaging）数据集之间保持保守。进一步的数据分析显示，斯蒂芬森滨海葵的枪丝（acontia）可能在转录层面无活性，且仅成熟的刺细胞存在于丝的远端部分。总体而言，本研究发现海葵不同解剖区域的毒液谱会根据其对应的生态功能而发生特异性变化。