Molecular evolution of K+ channels in primitive eukaryotes.

Abstract

Cnidarians and ciliate protozoans represent evolutionary interesting phylogenetic groups for the study of K+ channel evolution. Cnidaria is a primitive metazoan phylum consisting of simple diploblast organisms which have few tissue types such as jellyfish, hydra, sea anemones, and corals. Their divergence from the rest of the metazoan line may predate the radiation of the major triploblast phyla by several hundred million years (Morris, 1993). Cnidarians are the most primitive metazoans to have an organized nervous system. Thus, comparing K+ channels cloned from cnidarians to those cloned from more advanced metazoans may reveal which types of K+ channel are most fundamental to electrical excitability in the nervous system. In contrast, channels in ciliate protozoans such as Paramecium may not have been designed to send electrical signals between cells, but simply to control the behavior, such as an avoidance reaction, of a single cell. Hence, comparing cloned Paramecium K+ channels to K+ channels cloned from cnidarians and other metazoans may reveal which types of K+ channel are most fundamental to electrical excitability in eukaryotes, and which K+ channels are specialized for neuronal signaling. Potassium channels are involved in a diversity of tasks and are universally present in eukaryotes. K+ channels set the resting membrane potentials of most metazoan and protozoan cells and are fundamental components of membrane electrical activity in virtually all eukaryotic systems. These channels control the shape, duration and frequency of metazoan action potentials and are known to participate in the action potentials of protozoans, fungi and plants as well (Hille, 1992). Voltage-clamp recordings have shown that a various assortment of voltage-gated K+ channels as well as Ca(2+)-activated K+ channels are widespread in eukaryotes (Hille, 1992). Thus, K+ channels appear to be crucial to behavioral responses in all classes of eukaryotes, including locomotion in metazoans and protozoans, and rapid growth responses and cell shape changes in plants. K+ channel diversity is by far the greatest in metazoans, which have made a strong commitment to electrically excitable cellular networks. There is an apparent need for a great diversity of K+ channel subtypes in these metazoans. Over 50 K+ channel sequences from many distinct gene families have been reported so far, and all but two (both from plants) have been found in triploblast metazoans. The complex needs of neuronal integration and neuromuscular transmission in triploblasts require exquisite control of cellular excitability. This is in large part achieved by an extensive and diverse set of K+ channels.(ABSTRACT TRUNCATED AT 250 WORDS)