  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.
