Alternative mechanisms for fast Na⁺/Ca²⁺ signaling in eukaryotes via a novel class of single-domain voltage-gated channels

Abstract

Rapid Na ⁺ /Ca ²⁺ -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 ²⁺ channels (4D-Ca _v s/Na _v s). These channels are widely distributed across eukaryote diversity [4], albeit several eukaryotes, including land plants and fungi, have lost voltage-sensitive 4D-Ca _v /Na _v s [5–7]. Because these lineages appear to lack rapid Na ⁺ /Ca ²⁺ -based action potentials, 4D-Ca _v /Na _v s are generally considered necessary for fast Na ⁺ /Ca ²⁺ -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 _v /Na _v s [4] but also proteins of unknown function, resembling prokaryote single-domain, voltage-gated Na ⁺ channels (BacNa _v s) [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 ²⁺ -permeable channels, with rapid kinetics resembling metazoan 4D-Ca _v s/Na _v s. In Phaeodactylum tricornutum, which lacks 4D-Ca _v /Na _v s, EukCatAs underpin voltage-activated Ca ²⁺ signaling important for membrane excitability, and mutants exhibit impaired motility. EukCatAs therefore provide alternative mechanisms for rapid Na ⁺ /Ca ²⁺ signaling in eukaryotes and may functionally replace 4D-Ca _v s/Na _v s in pennate diatoms. Marine phytoplankton thus possess unique signaling mechanisms that may be key to environmental sensing in the oceans. Diatoms exhibit fast animal-like action potentials, but many species lack 4D-Ca _v /Na _v channels that underpin membrane excitability in animals. Diatoms do encode novel 1D voltage-gated channels (EukCatAs). Helliwell, Chrachri et al. show that EukCatAs are fast Na ⁺ and Ca ²⁺ channels that provide alternative mechanisms for rapid signaling in eukaryotes.

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