Abstract

Voltage-gated potassium channels (Kv) and cyclic nucleotide-binding domain-containing cation channels HCN, CNG, and KCNH are the evolutionarily related families of ion channels in animals. Their homologues were found in several lineages of eukaryotes and prokaryotes; however, the actual phylogenetic and structural diversity of these ion channels remains unclear. In this work, we present a taxonomically broad investigation of evolutionary relationships and structural diversity of Kv, HCN, CNG, and KCNH and their homologues in eukaryotes focusing on channels from different protistan groups. We demonstrate that both groups of channels consist of a more significant number of lineages than it was shown before, and these lineages can be grouped in two clusters termed Kv-like channels and CNBD-channels. Moreover, we, for the first time, report the unusual two-repeat tandem Kv-like channels and CNBD-channels in several eukaryotic groups, i.e. dinoflagellates, oomycetes, and chlorarachniophytes. Our findings reveal still underappreciated phylogenetic and structural diversity of eukaryotic ion channel lineages.

Highlights

  • Voltage-gated potassium channels ­(Kv) and cyclic nucleotide-binding domain-containing cation channels HCN, CNG, and KCNH are the evolutionarily related families of ion channels in animals

  • 262 homologues of ­Kv, KCNH, CNG, and HCN channels from 19 groups of eukaryotes, as well as several bacterial and archeal channels were chosen for the phylogenetic analysis (269 homologues and 302 sequences including separated repeats of the tandem channels) (Supplementary Table S1)

  • The phylogenetic analysis revealed that all ion channels considered in this work can be assigned to one of the two groups: (1) K­ v-like channels containing metazoan K­ v channel family among other K­ v-like channel clades, and (2) cyclic nucleotidebinding domain (CNBD)-channels containing familiar HCN, CNG, KCNH, and CNGK channels among other CNBD-channel clades (Fig. 3)

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Summary

Introduction

Voltage-gated potassium channels ­(Kv) and cyclic nucleotide-binding domain-containing cation channels HCN, CNG, and KCNH are the evolutionarily related families of ion channels in animals. Their homologues were found in several lineages of eukaryotes and prokaryotes; the actual phylogenetic and structural diversity of these ion channels remains unclear. We present a taxonomically broad investigation of evolutionary relationships and structural diversity of ­Kv, HCN, CNG, and KCNH and their homologues in eukaryotes focusing on channels from different protistan groups. CNBD-channels were identified in bacteria and were characterised as potassium-selective cyclic nucleotide-gated c­ hannels[22,23], but their physiological role in these organisms remains enigmatic

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