Abstract
All living cells interact dynamically with a constantly changing world. Eukaryotes, in particular, evolved radically new ways to sense and react to their environment. These advances enabled new and more complex forms of cellular behaviour in eukaryotes, including directional movement, active feeding, mating, and responses to predation. But what are the key events and innovations during eukaryogenesis that made all of this possible? Here we describe the ancestral repertoire of eukaryotic excitability and discuss five major cellular innovations that enabled its evolutionary origin. The innovations include a vastly expanded repertoire of ion channels, the emergence of cilia and pseudopodia, endomembranes as intracellular capacitors, a flexible plasma membrane and the relocation of chemiosmotic ATP synthesis to mitochondria, which liberated the plasma membrane for more complex electrical signalling involved in sensing and reacting. We conjecture that together with an increase in cell size, these new forms of excitability greatly amplified the degrees of freedom associated with cellular responses, allowing eukaryotes to vastly outperform prokaryotes in terms of both speed and accuracy. This comprehensive new perspective on the evolution of excitability enriches our view of eukaryogenesis and emphasizes behaviour and sensing as major contributors to the success of eukaryotes.This article is part of the theme issue ‘Basal cognition: conceptual tools and the view from the single cell’.
Highlights
Cellular excitability is the capacity to generate dynamic responses to stimuli, often over millisecond timescales
Different eukaryotic lineages are characterized by unique combinations of feeding modalities, control pathways and organization of motility appendages
We have identified specific yet universal changes in cellular and membrane architecture that we propose were crucial for such organisms to overcome many of the challenges associated with life and survival
Summary
Cellular excitability is the capacity to generate dynamic responses to stimuli, often over millisecond timescales. An excitable system often undergoes a characteristic excursion through state space, before returning to its original state after a refractory period has elapsed We invoke this extended definition of excitability to explore cellular phenomena that drive whole-organism behaviour across prokaryotic and eukaryotic cells. Excitability emerges as a biophysical consequence of charge separation across biological membranes This is regulated by the passage of ions between different cellular compartments through ion channels or biochemical signals initiated by metabotropic receptors. We proceed to argue that beyond changes in gene complements, several major cellular innovations were likely critical to the emergence of these new forms of behaviour These all evolved during eukaryogenesis and were likely to have been present in the last eukaryotic common ancestor (LECA). As Henri Poincaré once suggested ‘Le savant doit ordonner ... ’ [4]
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