Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK; Biosciences, College of Life and Environmental Sciences, Geoffrey Pope Building, University of Exeter, Exeter EX4 4QD, UK.
Marine Biological Association, The Laboratory, Citadel Hill, Plymouth PL1 2PB, UK.
Curr Biol. 2019 May 6;29(9):1503-1511.e6. doi: 10.1016/j.cub.2019.03.041. Epub 2019 Apr 18.
Rapid Na/Ca-based action potentials govern essential cellular functions in eukaryotes, from the motile responses of unicellular protists, such as Paramecium [1, 2], to complex animal neuromuscular activity [3]. A key innovation underpinning this fundamental signaling process has been the evolution of four-domain voltage-gated Na/Ca channels (4D-Cas/Nas). These channels are widely distributed across eukaryote diversity [4], albeit several eukaryotes, including land plants and fungi, have lost voltage-sensitive 4D-Ca/Nas [5-7]. Because these lineages appear to lack rapid Na/Ca-based action potentials, 4D-Ca/Nas are generally considered necessary for fast Na/Ca-based signaling [7]. However, the cellular mechanisms underpinning the membrane physiology of many eukaryotes remain unexamined. Eukaryotic phytoplankton critically influence our climate as major primary producers. Several taxa, including the globally abundant diatoms, exhibit membrane excitability [8-10]. We previously demonstrated that certain diatom genomes encode 4D-Ca/Nas [4] but also proteins of unknown function, resembling prokaryote single-domain, voltage-gated Na channels (BacNas) [4]. Here, we show that single-domain channels are actually broadly distributed across major eukaryote phytoplankton lineages and represent three novel classes of single-domain channels, which we refer collectively to as EukCats. Functional characterization of diatom EukCatAs indicates that they are voltage-gated Na- and Ca-permeable channels, with rapid kinetics resembling metazoan 4D-Cas/Nas. In Phaeodactylum tricornutum, which lacks 4D-Ca/Nas, EukCatAs underpin voltage-activated Ca signaling important for membrane excitability, and mutants exhibit impaired motility. EukCatAs therefore provide alternative mechanisms for rapid Na/Ca signaling in eukaryotes and may functionally replace 4D-Cas/Nas in pennate diatoms. Marine phytoplankton thus possess unique signaling mechanisms that may be key to environmental sensing in the oceans.
快速的 Na/Ca 动作电位控制着真核生物的基本细胞功能，从单细胞原生动物如草履虫的运动反应[1,2]，到复杂的动物神经肌肉活动[3]。这个基本信号过程的一个关键创新是进化出了四域电压门控 Na/Ca 通道（4D-Cas/Nas）。这些通道在真核生物多样性中广泛分布[4]，尽管包括陆地植物和真菌在内的几种真核生物已经失去了电压敏感的 4D-Ca/Nas[5-7]。由于这些谱系似乎缺乏快速的 Na/Ca 动作电位，因此 4D-Ca/Nas 通常被认为是快速 Na/Ca 信号所必需的[7]。然而，许多真核生物的膜生理学的细胞机制仍未被研究。真核浮游植物作为主要的初级生产者，对我们的气候具有重要影响。包括全球丰富的硅藻在内的几个类群表现出膜兴奋性[8-10]。我们之前证明，某些硅藻基因组编码 4D-Ca/Nas[4]，但也编码功能未知的蛋白质，类似于原核生物的单域电压门控 Na 通道（BacNas）[4]。在这里，我们表明单域通道实际上广泛分布于主要的真核浮游植物谱系中，并代表了三类新的单域通道，我们统称为 EukCats。硅藻 EukCatAs 的功能表征表明它们是电压门控的 Na 和 Ca 通透性通道，具有类似于后生动物 4D-Cas/Nas 的快速动力学。在缺乏 4D-Ca/Nas 的 P. tricornutum 中，EukCatAs 为电压激活的 Ca 信号提供基础，该信号对于膜兴奋性很重要，突变体表现出运动能力受损。因此，EukCatAs 为真核生物中快速的 Na/Ca 信号提供了替代机制，并且可能在有鞭毛的硅藻中替代 4D-Cas/Nas。海洋浮游植物因此拥有独特的信号机制，这可能是海洋环境感应的关键。
