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Abstract
Eukaryotic cells convert external stimuli into membrane depolarization, which in turn triggers effector responses such as secretion and contraction. Here, we put forward an evolutionary hypothesis for the origin of the depolarization–contraction–secretion (DCS) coupling, the functional core of animal neuromuscular circuits. We propose that DCS coupling evolved in unicellular stem eukaryotes as part of an ‘emergency response’ to calcium influx upon membrane rupture. We detail how this initial response was subsequently modified into an ancient mechanosensory–effector arc, present in the last eukaryotic common ancestor, which enabled contractile amoeboid movement that is widespread in extant eukaryotes. Elaborating on calcium-triggered membrane depolarization, we reason that the first action potentials evolved alongside the membrane of sensory-motile cilia, with the first voltage-sensitive sodium/calcium channels (Nav/Cav) enabling a fast and coordinated response of the entire cilium to mechanosensory stimuli. From the cilium, action potentials then spread across the entire cell, enabling global cellular responses such as concerted contraction in several independent eukaryote lineages. In animals, this process led to the invention of mechanosensory contractile cells. These gave rise to mechanosensory receptor cells, neurons and muscle cells by division of labour and can be regarded as the founder cell type of the nervous system.
Highlights
The intracellular composition of all living cells differs radically from that of extracellular fluids: the cytoplasm is richer in potassium, poorer in sodium— and, in particular, much poorer in calcium [2,3]
Membrane repair by exocytosis is observed in animals [66,67] and in plants [68,69,70]. We propose that this wound healing response dates back to the last eukaryotic common ancestor (LECA) and was the first manifestation of a tight coupling of depolarization, contraction and secretion, referred to here as DCS coupling
We propose that the step in the evolution of eukaryote DCS coupling has been the recruitment of stretch-sensitive calcium channels, which allow controlled influx of calcium upon mechanical stress before the actual damage occurs, and anticipate the effects of membrane rupture
Summary
The intracellular composition of all living cells differs radically from that of extracellular fluids: the cytoplasm is richer in potassium, poorer in sodium— and, in particular, much poorer in calcium (which does not exceed 1027 M in the resting cell but reaches 1023 and 1022 M in blood and seawater, respectively) [2,3]. The peculiar chemistry of the cytoplasm is often assumed to reflect the environment of the first cells [4,5] Based on their reconstituted membrane composition (rich in simple single-chain lipids), primitive cells were probably leaky to small molecules—their intracellular ionic balance necessarily matching the one of their environment [6,7]. The most prominent are active sodium and calcium efflux pumps: Naþ and Ca2þ efflux ATPases are widespread in both eukaryotes and prokaryotes, and are probable ancestral features of all living cells [11,12,13,14,15,16,17,18,19] Another shared strategy is concentration of calcium in specialized storage spaces, both intracellular [20 –24] and extracellular, like cell walls or skeletal structures [10,25,26]. Differential distribution of these functions among distinct cell types by division of labour gave rise to the configuration of modern neuronal and neuromuscular circuits in animals
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Schedule a callMore From: Philosophical Transactions of the Royal Society B: Biological Sciences
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