Early Evolution of the Eukaryotic Ca2+ Signaling Machinery: Conservation of the CatSper Channel Complex

Abstract

Calcium signaling is one of the most extensively employed signal transduction mechanisms in life. As life evolved into increasingly complex organisms, Ca2+ acquired more extensive and varied functions. Here we compare genes encoding proteins that govern Ca2+ entry and exit across cells or organelles within organisms of early eukaryotic evolution into fungi, plants, and animals. Recent phylogenomics analyses reveal a complex Ca2+ signaling machinery in the apusozoan protist Thecamonas trahens, a putative unicellular progenitor of Opisthokonta. We compare T. trahens Ca2+ signaling to that in a marine bikont protist, Aurantiochytrium limacinum, and demonstrate the conservation of key Ca2+ signaling molecules in the basally diverging alga Cyanophora paradoxa. Particularly, our findings reveal the conservation of the CatSper channel complex in A. limacinum and C. paradoxa, suggesting that the CatSper complex likely originated from an ancestral Ca2+ signaling machinery at the root of early eukaryotic evolution prior to the unikont/bikont split.

Tracing the Evolutionary History of Inositol, 1, 4, 5-Trisphosphate Receptor: Insights from Analyses ofCapsaspora owczarzakiCa2+Release Channel Orthologs

“…However, the origin and history of IP 3 R and RyR remains poorly defined. Nevertheless, it has recently been shown that many components of Ca 2+ signaling machinery are encoded in the genomes of many unicellular eukaryotes (Cai 2008; Cai and Clapham 2008, 2012; Cai, et al 2014). Whether, or how, unicellular IP 3 R and RyR-mediated signaling have contributed to the evolution and success of multicellular organisms is presently unknown.…”

“…However, several recent bioinformatics and phylogenetic studies that surveyed the sequenced genomes of a diverse array of unicellular eukaryotic species have revealed a rich repertoire of genes encoding proteins predicted to be involved in Ca 2+ signaling and which had previously been widely presumed to be unique to higher animals (Cai 2008; Cai and Clapham 2008, 2012; Cai, et al 2014). Although these studies have highlighted sequence conservation of a number of components of the unicellular Ca 2+ machinery, functional verification of the annotated genes is still lacking.…”

Melatonin increases intracellular calcium in the liver, muscle, white adipose tissues and pancreas of diabetic obese rats

“…16 Furthermore, several studies have demonstrated that age-related insulin secretion dysfunction plays an important role in glucose metabolism disorders at older ages, contributing to the high indexes of glucose intolerance in elderly populations. 20 Ca 2+ was found to play a key role in β-cell functionality, 21 and a lower intracellular level of Ca 2+ was associated with the presence of hyperglycemia and a depolarizing K + stimulus. 20 Ca 2+ was found to play a key role in β-cell functionality, 21 and a lower intracellular level of Ca 2+ was associated with the presence of hyperglycemia and a depolarizing K + stimulus.…”

The Glaucophyta: the blue-green plants in a nutshell

“…Some examples are the genes encoding the mitochondrialtargeted porin Mdm10, which is part of the endoplasmic reticulum-mitochondria encounter structure (ERMES) [98], and proteins involved in the calcium signaling machinery (Ca 2+ SM), such as CatSper-like (cation channels of sperm), CaV (membrane voltage-gated Ca 2+ ) and TRP (transient receptor potential) channels [99]. The presence of the ERMES and the Ca 2+ SM in diverse major eukaryotic groups, now including glaucophytes, suggest an ancient origin of these pathways.…”