Apusomonad photophobic behavior highlights cytoskeletal responses to blue light in early eukaryotes

Abstract

Light response is a fundamental characteristic of eukaryotic organisms, both unicellular and multicellular. However, no photoresponse has previously been reported in Apusomonadida, a group of small, free-living biflagellates phylogenetically positioned as a sister group to Opisthokonta (animals, fungi, and their unicellular relatives). Apusomonads are thus crucial for understanding the evolution of opisthokonts. Here, we report for the first time an avoidance response to blue light in the apusomonad Podomonas kaiyoae. This avoidance response is accompanied by an increase in gliding velocity, transient changes in flagellar waveforms, and alterations in cell shape. Dynamic cell contraction is induced by an increase in intracellular free Ca2+ and is inhibited by either a dynein inhibitor or an actin-disrupting drug. These findings suggest that the photophobic behavior of Podomonas kaiyoae relies on cytoskeletal responses mediated by both the dynein/tubulin and myosin/actin systems, which were acquired early in eukaryotic evolution. The dominance of the posterior flagellum in cilia-driven directional changes further supports the phylogenetic placement of apusomonads as a sister group to opisthokonts rather than other eukaryotic lineages.