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 behavior in eukaryotes, including directional movement, active feeding, mating, or 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, endomembranes as intracellular capacitors, a flexible plasma membrane, the emergence of cilia and pseudopodia, and the relocation of chemiosmotic ATP synthesis to mitochondria that liberated the plasma membrane for more complex electrical signaling 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.
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