Simonson Benjamin T, Jiang Zhaoyang, Ryan Joseph F, Jegla Timothy
Department of Biology and Huck Institutes of the Life Sciences, Penn State University, University Park, PA, USA.
Whitney Laboratory for Marine Bioscience, University of Florida , St. Augustine, FL, USA.
J Gen Physiol. 2025 May 5;157(3). doi: 10.1085/jgp.202413740. Epub 2025 Mar 18.
The ctenophore species Mnemiopsis leidyi is known to have a large set of voltage-gated K+ channels, but little is known about the functional diversity of these channels or their evolutionary history in other ctenophore species. Here, we searched the genomes of two additional ctenophore species, Beroe ovata and Hormiphora californensis, for voltage-gated K+ channels and functionally expressed a subset of M. leidyi channels. We found that the last common ancestor of these three disparate ctenophore lineages probably had at least 33 voltage-gated K+ channels. Two of these genes belong to the EAG family, and the remaining 31 belong to the Shaker family and form a single clade within the animal/choanoflagellate Shaker phylogeny. We additionally found evidence for 10 of these Shaker channels in a transcriptome of the early branching ctenophore lineage Euplokamis dunlapae, suggesting that the diversification of these channels was already underway early in ctenophore evolution. We functionally expressed 16 Mnemiopsis Shakers and found that they encode a diverse array of voltage-gated K+ conductances with functional orthologs for many classic Shaker family subtypes found in cnidarians and bilaterians. Analysis of Mnemiopsis transcriptome data show these 16 Shaker channels are expressed in a wide variety of cell types, including neurons, muscle, comb cells, and colloblasts. Ctenophores therefore appear to have independently evolved much of the voltage-gated K+ channel diversity that is shared between cnidarians and bilaterians.
栉水母物种海胡桃(Mnemiopsis leidyi)已知拥有大量电压门控钾通道,但对于这些通道的功能多样性或它们在其他栉水母物种中的进化历史却知之甚少。在这里,我们在另外两种栉水母物种——卵形帆水母(Beroe ovata)和加州海醋栗(Hormiphora californensis)的基因组中搜索电压门控钾通道,并对海胡桃的一部分通道进行了功能表达。我们发现,这三个不同的栉水母谱系的最后一个共同祖先可能至少有33种电压门控钾通道。其中两个基因属于EAG家族,其余31个属于Shaker家族,并在动物/领鞭毛虫Shaker系统发育中形成一个单独的进化枝。我们还在早期分支的栉水母谱系邓氏真瘤水母(Euplokamis dunlapae)的转录组中发现了其中10个Shaker通道的证据,这表明这些通道的多样化在栉水母进化早期就已经开始了。我们对16个海胡桃Shaker通道进行了功能表达,发现它们编码了多种电压门控钾电导,与刺胞动物和两侧对称动物中发现的许多经典Shaker家族亚型具有功能同源物。对海胡桃转录组数据的分析表明,这16个Shaker通道在多种细胞类型中表达,包括神经元、肌肉、栉板细胞和粘细胞。因此,栉水母似乎独立进化出了许多刺胞动物和两侧对称动物共有的电压门控钾通道多样性。