Deployment of hagfish slime thread skeins requires the transmission of mixing forces via mucin strands

Hagfishes are benthic marine protovertebrates that secrete copious quantities of slime when threatened. The slime originates as a two-component glandular exudate comprised of coiled bundles of cytoskeletal intermediate filaments (thread skeins) and mucin vesicles. Holocrine secretion of the slime into seawater results in the rapid deployment of both fibrous and mucin components, resulting in about a liter of dilute slime. Deployment of the thread skeins involves their unraveling in a fraction of a second from a 150 mm-long ellipsoid bundle to a thread that is 100X longer. We hypothesized that thread skein deployment requires both vigorous hydrodynamic mixing and the presence of mucin vesicles, both of which are required for whole slime deployment. Here we provide evidence that mixing and mucin vesicles are indeed crucial for skein unraveling. Specifically, we show that mucin vesicles mixed into seawater swell and elongate into high-aspect ratio mucin strands that attach to the thread skeins, transmit hydrodynamic forces to them and effect their unraveling by loading them in tension. Our discovery of mucin strands in hagfish slime not only provides a mechanism for the rapid deployment of thread skeins in vivo, it also helps explain how hagfish slime is able to trap such impressive volumes of seawater via viscous entrainment. We believe that the deployment of thread skeins via their interaction with shear-elongated mucins represents a unique mechanism in biology and may lead to novel technologies for transmitting hydrodynamic forces to microscale particles that would typically be immune to such forces.