Spontaneous unraveling of hagfish slime thread skeins is mediated by a seawater-soluble protein adhesive

Abstract

Hagfishes are known for their ability to rapidly produce vast quantities of slime when provoked. The slime is formed via the interaction between seawater and two components released by the slime glands: mucin vesicles from gland mucous cells, which swell and rupture in seawater to form a network of mucus strands, and intermediate filament-rich threads, which are produced within gland thread cells as tightly coiled bundles called skeins. A previous study showed that the unraveling of skeins from Atlantic hagfish (Myxine glutinosa) requires both the presence of mucins and hydrodynamic mixing. In contrast, skeins from Pacific hagfish (Eptatretus stoutii) unravel in the absence of both mucins and mixing. We tested the hypothesis that spontaneous unraveling of E. stoutii skeins is triggered by the dissolution of a seawater-soluble protein adhesive and the release of stored strain energy within the coiled thread. Here we show that, as predicted by this hypothesis, unraveling can be initiated by a protease under conditions in which unraveling does not normally occur. We also demonstrate, using high resolution scanning electron microscopy, that the treatment of skeins with solutions that cause unraveling also leads to the disappearance of surface and inter-thread features that remain when skeins are washed with stabilizing solutions. Our study provides a mechanism for the deployment of thread skeins in Pacific hagfish slime, and raises the possibility of producing novel biomimetic protein adhesives that are salt, temperature and kosmotrope sensitive.

Unravelling hagfish slime

“…Although the physiological flow fields may be different from the ones that were used in the analysis, our results underline the importance of viscous hydrodynamics and boundary conditions on the process. Recent work [11] found that Pacific hagfish skeins undergo spontaneous unravelling in salt solution. However, the observed unravelling time scales ( min) are much larger than the physiological time scales (approx.…”

“…The secreted biomaterial has two main constituents-gland mucus cells and gland thread cells-responsible for the mucus and fibrous component of slime, respectively [6,10]. The plasma membranes of both kinds of cells shear off when secreted from the slime glands [10,11]. In the present study, we focus on the secreted thread cells, referred to as skeins from here on.…”

Yarının Yüksek Performanslı Liflerine Doğal Bir Yaklaşım: Balık Asalağı Salgısı Lifleri

“…Saç gibi doğal keratin içerikli protein lifinin çok hücreli yapılarının aksine balık asalağı salgısı lifleri tek bir hücre içerisinde oluşur [9,25]. [12,20,34]. Ara filamentlerin oluşturduğu lif yumaklarındaki çözülmenin maksimum olduğu şartlar 5-10 o C arası, 1.25 M sodyum klorit konsantrasyonu olarak kaydedilmiştir [34].…”

“…[12,20,34]. Ara filamentlerin oluşturduğu lif yumaklarındaki çözülmenin maksimum olduğu şartlar 5-10 o C arası, 1.25 M sodyum klorit konsantrasyonu olarak kaydedilmiştir [34].…”

Structure and dynamics of hagfish mucin in different saline environments

“…The fact that a charged gel with a complex network structure rapidly deploys in a strongly charge-screening environment as in seawater (ionic strength of about 0.7 M 12 ) is intriguing and has led to studies that investigated the effects of ionic strength and ionic composition. The main areas of focus comprised the effects of salts on ex vivo stabilization of hagfish exudate, 8,[13][14][15] skein unraveling, 16,17 mucin vesicle swelling and rupture, 9,[16][17][18] swelling and hydration of skeins 19 and reconstituted biomimetic materials made from slime thread proteins, 20 and whole hagfish slime functionality. 17 These studies show (i) that a high osmolarity of about 800 mOsmol l À1 and higher achieved by divalent anions (sulfate, citrate, phosphate) stabilizes hagfish exudate, 8,14,15 (ii) that seawater assists the dissolution of a glue, which holds the native skeins together and mediates unraveling, 16 (iii) that protein threads and materials made from those protein swell less in high osmolarity environments, 19,20 (iv) that viscosities of mucin solutions are lower in seawater than in deionized water, 11,17 and (v) that swelling and rupture of hagfish mucin vesicles requires the presence calcium ions when the ionic strength of the solution is 4100 mM.…”