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Alternative mechanisms for fast Na + /Ca 2+ signaling in eukaryotes via a novel class of single-domain voltage-gated channels

Alternative mechanisms for fast Na + /Ca 2+ signaling in eukaryotes via a novel class of single-domain voltage-gated channels
Alternative mechanisms for fast Na + /Ca 2+ signaling in eukaryotes via a novel class of single-domain voltage-gated channels

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.

action potentials, BacNa, calcium channel, diatoms, EukCats, gliding motility, ion selectivity, signaling, single-domain channel, voltage-gated channel
0960-9822
1503-1511.e6
Helliwell, Katherine E.
514f8174-da3f-46c8-be0d-3bcd92ee8189
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Koester, Julie A.
b667b66c-d284-4be5-bedf-338a27be02a9
Wharam, Susan
1d37eedf-556e-4b1e-94d5-465e2a3e6e01
Verret, Frédéric
cabbad28-63b7-4011-aeee-6e1bc74c2da1
Taylor, Alison R.
a20791ff-9a08-4fb9-b484-2e39368f7789
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385
Helliwell, Katherine E.
514f8174-da3f-46c8-be0d-3bcd92ee8189
Chrachri, Abdul
4c8a3ca0-7e80-42f4-a3be-dd2dae8583ba
Koester, Julie A.
b667b66c-d284-4be5-bedf-338a27be02a9
Wharam, Susan
1d37eedf-556e-4b1e-94d5-465e2a3e6e01
Verret, Frédéric
cabbad28-63b7-4011-aeee-6e1bc74c2da1
Taylor, Alison R.
a20791ff-9a08-4fb9-b484-2e39368f7789
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385

Helliwell, Katherine E., Chrachri, Abdul, Koester, Julie A., Wharam, Susan, Verret, Frédéric, Taylor, Alison R., Wheeler, Glen L. and Brownlee, Colin (2019) Alternative mechanisms for fast Na + /Ca 2+ signaling in eukaryotes via a novel class of single-domain voltage-gated channels. Current Biology, 29 (9), 1503-1511.e6. (doi:10.1016/j.cub.2019.03.041).

Record type: Article

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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Accepted/In Press date: 20 March 2019
e-pub ahead of print date: 18 April 2019
Published date: 6 May 2019
Keywords: action potentials, BacNa, calcium channel, diatoms, EukCats, gliding motility, ion selectivity, signaling, single-domain channel, voltage-gated channel

Identifiers

Local EPrints ID: 430721
URI: https://eprints.soton.ac.uk/id/eprint/430721
ISSN: 0960-9822
PURE UUID: a89b8695-b1d7-48cb-bdd4-d6f364f2952d

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Date deposited: 09 May 2019 16:30
Last modified: 02 Dec 2019 17:37

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