Calcium Regulation in the Protozoan Model, Paramecium tetraurelia

Abstract

Early in eukaryotic evolution, the cell has evolved a considerable inventory of proteins engaged in the regulation of intracellular Ca(2+) concentrations, not only to avoid toxic effects but beyond that to exploit the signaling capacity of Ca(2+) by small changes in local concentration. Among protozoa, the ciliate Paramecium may now be one of the best analyzed models. Ciliary activity and exo-/endocytosis are governed by Ca(2+) , the latter by Ca(2+) mobilization from alveolar sacs and a superimposed store-operated Ca(2+) -influx. Paramecium cells possess plasma membrane- and endoplasmic reticulum-resident Ca(2+) -ATPases/pumps (PMCA, SERCA), a variety of Ca(2+) influx channels, including mechanosensitive and voltage-dependent channels in the plasma membrane, furthermore a plethora of Ca(2+) -release channels (CRC) of the inositol 1,4,5-trisphosphate and ryanodine receptor type in different compartments, notably the contractile vacuole complex and the alveolar sacs, as well as in vesicles participating in vesicular trafficking. Additional types of CRC probably also occur but they have not been identified at a molecular level as yet, as is the equivalent of synaptotagmin as a Ca(2+) sensor for exocytosis. Among established targets and sensors of Ca(2+) in Paramecium are calmodulin, calcineurin, as well as Ca(2+) /calmodulin-dependent protein kinases, all with multiple functions. Thus, basic elements of Ca(2+) signaling are available for Paramecium.

Evolution of voltage-gated ion channels at the emergence of Metazoa

“…2+ currents are associated with locomotion via flagellar movements in paramecium (Plattner, 2014) and algae (Chlamydomonas) (Wakabayashi et al, 2009;Fujiu et al, 2009), stress responses in diatoms (Vardi et al, 2006), protein secretion, motility differentiation and infection in parasitic protozoa (Moreno and Docampo, 2003;Nagamune et al, 2007) and light emission in dinoflagellates (von Dassow and Latz, 2002). Hence, it would seem that four-domain Ca V s would be widespread in protozoa.…”

“…Phylogeny reveals that NvErg1 and the mammalian channels represent the ancestral electrical behavior, whereas NvErg4 evolved in a convergent manner to the Drosophila channel. Surprisingly, it seems that nematode Erg channels also acquired this feature independently, suggesting that this electrical behavior evolved at least three times during animal evolution (Martinson et al, 2014).Voltage-gated calcium channels: a widely, yet sparsely, distributed channel family Ca 2+ currents are associated with locomotion via flagellar movements in paramecium (Plattner, 2014) and algae (Chlamydomonas) (Wakabayashi et al, 2009;Fujiu et al, 2009), stress responses in diatoms (Vardi et al, 2006), protein secretion, motility differentiation and infection in parasitic protozoa (Moreno and Docampo, 2003;Nagamune et al, 2007) and light emission in dinoflagellates (von Dassow and Latz, 2002). Hence, it would seem that four-domain Ca V s would be widespread in protozoa.…”

Inseparable tandem: evolution chooses ATP and Ca2+to control life, death and cellular signalling

“…H þ /Ca 2þ exchangers or related antiporters), all to be found in the plasmalemma and in the endomembranes [20,22,76,77]; intracellular Ca 2þ dynamics is further regulated by Ca 2þ buffers [56]. All these mechanisms were invented early in evolution, be it in ancestors of unikonts, such as choanoflagellates [78], or be it in bikonts, such as ciliates [38,40]. Cytosol contains both mobile and immobile Ca 2þ buffers of different capacity and affinity.…”

“…An exception is the ciliate, Paramecium, where a rapidly activated SOCE underlies the fastest known exocytosis of dense core-secretory vesicles important for predator defence [40,135]. The final target of Ca 2þ during any type of secretion is the C2-domain-bearing protein synaptotagmin, and closely related Ca 2þ -sensors, such as extended synaptotagmin isoforms of which several ( probably with different kinetics) are known [53].…”

Principles of Intracellular Signaling in Ciliated Protozoa—A Brief Outline

“…Below Parallel situations seen on ultrathin sections. a Data pertinent to trichocyst processing are based on previous reviews (Plattner et al 1993;Plattner 2014), those for endo /phagocytotic trafficking are mainly derived from Allen and Fok (2000) and c trafficking in context of the contractile vacuole complex is based on recent reviews (Plattner 2015b(Plattner , 2016a b is modified from Plattner (2014), c is modified from Plattner et al (1993Plattner et al ( , 1997 and SU-B (regulatory SU, with Ca 2 +· binding domain) also in ciliates respective protein kinases, protein kinase A (PKA) and protein kinase G (PKG) (Bonini and Nelson 1990); for review see Plattner (2016a). Also some metabolic Ca 2 + channel activators, such as cyclic adenosinediphosphoribose (cADPR) and nicotinic acid adenine cfmucleotidephosphate (NAADP) are derived from nucleotides, i.e.…”