Long-range actin-driven endosymbiont mobility in a deep-diverging bilaterian

Symbiosis is everywhere, and “we have never been individuals”[1, 2]. In animal-microbe symbioses, established symbionts are often thought to be confined to a specific cellular or tissue niche[3–7] and generally lose their motile appendages such as flagella[8–15]. However, whether the loss of motile appendages necessarily implies immobility within the animal host remains an open conundrum. Here, we present the discovery of long-range, host actin-driven symbiont mobility in a dinoflagellate-acoel worm symbiosis. Using long-term tracking, fluorescence, and electron microscopy, we find that dinoflagellate symbionts ( Amphidinium sp. , 10-20 µm in size) travel throughout an extensive network of thin host cells ( ∼ 200 nm in regions without symbionts) in Waminoa sp. acoel worms, which are part of a deep-diverging bilaterian lineage[16–18]. Although FIB-SEM-based 3D reconstruction shows symbionts still retain both flagella, we uncover that it is host actin machinery that plays a primary role in overcoming large drag forces under confinement to achieve mobility throughout the worm at surprisingly high velocities (around 1 µm/s ). Long term in-toto imaging further reveals diel rhythms and spatiotemporal regulation of symbionts during regeneration. Our findings show the presence of host-mediated mobility in animal-microbe symbioses, which suggests the existence of previously overlooked regulatory processes in holobionts’ maintenance of dynamic homeostasis.