Endocytobiotic Coordination, Intracellular Calcium Signaling, and the Origin of Endogenous Rhythms

Abstract

Elementary differences in the regulation of cellular physiology separate prokaryotic and eukaryotic organisms. As will be emphasized throughout this paper, fundamental disparities are already apparent at the unicellular level of eukaryotic organization. Regarding their universality in eukaryotes almost inevitably leads to the suggestion that some of these early acquisitions of the developing eukaryotic cell were of prominent evolutionary significance for the later emergence of eukaryotic complexity and diversity. The superior influence of interactions between cellular compartments on cellular evolution has been pointed out previously.' A more pervasive statement is the principal notion of this paper that those interactions culminating in mechanisms for the integration of today's semiautonomous organelles were even indispensable for the evolution of the eukaryotic cell out of an endocytobiotic organization. Hence, the endosymbiotic theory may not only account for the origin of mitochondria and plastids but equally for a substantial part of the developmental potency arising in conjunction with the first eukaryotic organisms. Two essential features of cell regulation ubiquitous in eukaryotes are suggested to have evolved as a consequence of mutual interactions between partners in a cellular symbiotic consortium developing towards the eukaryotic cell: endogenous rhythms and the calcium system of intracellular signaling. These two characters unique to eukaryotic cells may be intertwined, the calcium system being an integral part of the cellular clock mechanism.The presence of a nucleus as the defining characteristic of eukaryotic cells is at the same time the most easy means to distinguish them from their prokaryotic counterparts. Equally eyecatching are their usually much larger size and the complex structure of the cytoplasm harboring various organelles. Differences in cellular morphology like these have been dealt with extensively; likewise those in essential metabolic pathways and the biochemistry of subcellular components. More recently, differences in molecular biology between the two basic subdivisions of life have constituted an 476

Entrainment and Phase-Shifting of the Circadian Rhythm of Cell Division by Calcium in Synchronous Cultures of the Wild-Type Z Strain and of the ZC Achlorophyllous Mutant of Euglena gracilis

“…The question remains whether calcium is part ofthe oscillator itself ( 18,21,22) or is merely upstream (along the entrainment pathway) (19,20,25,26) or downstream (coupling the clock to its hands) from it (34,38). If intracellular calcium cycling, which has been hypothesized to trigger nuclear and cytoplasmic cycles (36), indeed is an element of the oscillator, the identity of the key compartments, as well as of other clock gears, awaits elucidation (13).…”

“…Indeed, it has been demonstrated in a variety of eukaryotic organisms that circadian rhythmicity of many different types of physiological processes are modulated by calcium levels: cell shape (23, 24) cell division (18) in Euglena gracilis, ocular rhythms in Bulla gouldiana (25), leaf movement in Trifolium repens (3) and Cassiafasciculata (29), conidiation in Neurospora crassa (27), and phototaxis in Chlamydomonas reinhardtii (17). Three models for circadian oscillators (10) that are based in part on cellular calcium (18,21,22) share in common a cycling ofintracellular calcium among compartments (endoplasmic reticulum, mitochondria, cytoplasm, extracellular medium-depending on the model). Although this intercompartmental calcium cycling in itself constitutes the circadian mechanism in the Kippert model (21), it is only one important element of a biochemical circadian loop in that of Goto et al (18).…”

“…Three models for circadian oscillators (10) that are based in part on cellular calcium (18,21,22) share in common a cycling ofintracellular calcium among compartments (endoplasmic reticulum, mitochondria, cytoplasm, extracellular medium-depending on the model). Although this intercompartmental calcium cycling in itself constitutes the circadian mechanism in the Kippert model (21), it is only one important element of a biochemical circadian loop in that of Goto et al. (18).…”

Bacterial Circadian Programs

“…The conjunction of structural information on essential clock proteins with a defined system that reconstitutes circadian oscillations in vitro leads to a turning point whereby biophysical and biochemical approaches bring analyses of circadian clockwork to an unprecedented level of molecular detail. conceived to be a necessary prerequisite for a circadian mechanism (Ehret and Trucco 1967;Schweiger and Schweiger 1977;Kippert 1986). During 1985-1986, three papers were published that began to depose the "no clocks in proks" dogma (Stal and Krumbein 1985;Grobbelaar et al 1986;Mitsui et al 1986).…”

“…conceived to be a necessary prerequisite for a circadian mechanism (Ehret and Trucco 1967;Schweiger and Schweiger 1977;Kippert 1986). During 1985-1986, three papers were published that began to depose the "no clocks in proks" dogma (Stal and Krumbein 1985;Grobbelaar et al 1986;Mitsui et al 1986). These various groups discovered that cyanobacteria which fix nitrogen (Oscillatoria sp.…”