Epidermal threads reveal the origin of hagfish slime
- Schmid College of Science and Technology, Chapman University, United States
- Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, United States
- Department of Evolution, Ecology and Organismal Biology, University of California at Riverside, United States
Figures
Figure 1 with 1 supplement
Mechanism and evolutionary history of hagfish slime.
(A) Hagfish defensive slime is produced by rapid ejection and rupture of mucous cells and thread cells into seawater by slime glands. Top shows a schematic sequence of slime formation. Threads and …
Figure 1—figure supplement 1
Cross-section of lamprey (Petromyzon marinus) epidermis based on hematoxylin-eosin (H&E)-stained cross-sectional slides.
Right shows a lamprey skein cell imaged with confocal laser scanning microscopy. The large fiber in lamprey skein cell ranges 80–120 and 30–60 μm in length and width, respectively (see also Lane and …
Figure 2 with 2 supplements
Morphology of the hagfish epidermal thread cell.
(A) Cross-section of dorsal epidermis from a Pacific hagfish (Eptatretus stoutii; hematoxylin-eosin-stained; bright-field microscopy). SMC, small mucous cell; LMC, large mucous cell; ETC, epidermal …
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Figure 2—source data 1
Density of epidermal cells.
- https://cdn.elifesciences.org/articles/81405/elife-81405-fig2-data1-v1.xlsx
Figure 2—figure supplement 1
Abundance of hagfish epidermal cells.
(A) Schematic showing anteroposterior position (PAP), with 0 representing the snout and 1 the tip of the tail. (Bottom left) Schematic showing dorsoventral positions (PDV) in a hagfish in …
Figure 2—figure supplement 2
Morphology of epidermal thread cell (ETC) at different developmental stages.
(A–D) Developmental sequence of ETCs represented by cells of different sizes, with smaller cells at the bottom. Each cell is shown with images stacks at different z-distance, as annotated on the …
Figure 3 with 1 supplement
Geometry of hagfish epidermal threads.
(A) Three levels of epidermal thread structure. (Left-middle) At the micro-scale, the thread traces a right-handed helix, the centerline of which is arranged in a switchback pattern on the inner …
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Figure 3—source data 1
Geometry of epidermal threads sampled using laser confocal microscopy.
- https://cdn.elifesciences.org/articles/81405/elife-81405-fig3-data1-v1.xlsx
Figure 3—figure supplement 1
Morphology of epidermal threads.
(A) Scanning electron microscopy (SEM) images showing details of a single epidermal thread cell (ETC) thread on the epidermal surface abraded with sandpaper, showing subfilament structure. (B) …
Figure 4 with 2 supplements
Size of released epidermal threads.
(A) A partially released thread (~2 mm long) from a ruptured epidermal thread cell (ETC), as viewed under light microscopy (see also Figure 4—figure supplement 1). (B) A thread with two free ends. (C…
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Figure 4—source data 1
Length of epidermal threads sampled using transmitted light microscopy.
- https://cdn.elifesciences.org/articles/81405/elife-81405-fig4-data1-v1.xlsx
Figure 4—figure supplement 1
Release of epidermal threads.
(A) Schematic of sampling epidermal mucus using a coverslip scraped along the skin of an anesthetized hagfish. The coverslip was only gently pressed against the hagfish skin, as shown on the right. …
Figure 4—figure supplement 2
Release of epidermal threads.
(A–B) Granule clusters found on the epidermal surface, with helical threads still attached. (C) Partially released epidermal thread cell (ETC) granule cluster found on the epidermal surface.
Figure 5
Comparison of distribution, size, and shape between epidermal and slime threads.
(A) A schematic comparison of the distribution of epidermal and gland thread cells, as well as the mean lengths and diameters of corresponding thread products. Data based on Pacific hagfish (Eptatret…
Figure 6 with 3 supplements
Formation and structure of epidermal slime produced by wounded skin.
(A) Schematic of epidermal slime formation when epidermis is wounded, with threads and granules from ruptured epidermal thread cells (ETCs) mixing with mucus from ruptured large mucous cells (LMCs). …
Figure 6—figure supplement 1
Formation of epidermal slime.
Newly wounded hagfish skin was fixed, dehydrated, and observed using scanning electron microscopy (SEM). (A–B) Formation of epidermal slime on abraded skin, with details showing the slime as a …
Figure 6—figure supplement 2
Structure of epidermal slime.
(A) Epidermal slime observed using differential interference contrast (DIC) microscopy, showing epidermal thread cell (ETC) threads, granules, and detached small mucous cells (SMC). (B) Epidermal …
Figure 6—figure supplement 3
Structure of epidermal slime.
(A–C) After scraping hagfish skin with rough surfaces (sand paper and wood), we observed epidermal slime adhered to these surfaces using scanning electron microscopy (SEM). The epidermal slime …
Figure 7 with 1 supplement
Water content and fibrosity of hagfish epidermal slime.
(A) The relative water content of epidermal slime collected by scraping a glass coverslip over blotted skin (unswollen) and underwater (swollen). Dots represent individual samples; colors represent …
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Figure 7—source data 1
Water content of epidermal slime sampled from hagfish skin (blot-dried in air versus underwater).
- https://cdn.elifesciences.org/articles/81405/elife-81405-fig7-data1-v1.xlsx
Figure 7—figure supplement 1
Morphometrics of hagfish defensive slime.
(A) Full glands and newly emptied glands on the same hagfish, showing difference in size and similarity in shape (see Schorno et al., 2018). We found that full and newly emptied glands share a …
Figure 8 with 2 supplements
Molecular analyses suggest an epidermal origin of hagfish defensive slime threads.
(A and B) Differentially expressed transcripts (red) from skin versus slime gland RNAseq datasets (3× replicates each, from single specimens of Eptatretus goslinei; FDR <0.001). In both species, a …
Figure 8—figure supplement 1
Phylogenetic analysis of vertebrate thread biopolymer alpha genes from selected taxa, rooted with its closest sister clade, which is comprised of type II keratins.
This tree was rooted with more distant outgroups that included glial acidic fibrillary protein and other neuronally expressed intermediate filament loci, not shown. Nodal support is given by …
Figure 8—figure supplement 2
Phylogenetic analysis of vertebrate thread biopolymer gamma genes from selected taxa, rooted with its closest sister clade, which is comprised of type I keratins.
This tree was rooted with more distant outgroups that included desmins and other distantly related skin expressed keratins, not shown. Nodal support is given by ultrafast bootstrap and approximate …
Figure 9
An epidermal origin of hagfish slime.
(A) A comparison of slime formation mechanism between epidermal and defensive slimes, highlighting their similarity in basic structural components and differences in mixing mechanism. Note a …
Videos
Video 1
Z-stack image sequences of eosin-stained hagfish epidermis from confocal laser scanning microscopy with transmitted light, taken in en face view.
Note a dense layer of epidermal thread cells (ETCs) and large mucous cells at the basal layer of epidermis. Each ETC is evident with a cluster of granules highlighted in red, while large mucous …
Video 2
Z-stack image sequences of hagfish epidermis from confocal laser scanning microscopy, taken in en face view.
Note the outermost epidermis is covered by a layer of small mucous cells, while epidermal thread cells (ETCs) are found at the basal layer.
Video 3
Z-stack image sequences of hagfish epidermal thread cells (ETCs) based on confocal laser scanning microscopy.
Images were taken from eosin-stained epidermis, and the ETC granules are the brightest feature.
Video 4
Three-dimensional reconstructions of epidermal thread cells (ETCs) based on confocal laser scanning microscopy, showing granule cluster and helical-shaped threads packed along the plasma membrane.
Video 5
Experimentally induced formation of epidermal slime, demonstrated by scraping wet and blot-dried hagfish skin with a sharp pin head.
Scraping with a blunt pinhead did not lead to slime formation.
Video 6
Different from condensed, adhesive hagfish epidermal slime, the defensive slime is highly diluted and not sticky.
Tables
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Gene (RNAseq data of hagfishes Eptatretus goslinei, Eptatretus stoutii) | Under BioProject PRJNA896978 at https://www.ncbi.nlm.nih.gov/sra | |||
| Biological sample (hagfishes: Eptatretus goslinei, Eptatretus stoutii) | Wild-captured | |||
| Software, algorithm | R (https://www.r-project.org/) | |||
| Software, algorithm | Code (https://github.com/plachetzki/ETC_GTC) |
Additional files
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MDAR checklist
- https://cdn.elifesciences.org/articles/81405/elife-81405-mdarchecklist1-v1.pdf
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Supplementary file 1
Supplementary table.
(A) Morphological parameters of slime glands of Pacific Hagfish. (B) Comparison of fibrosity between defensive slime and epidermal slime.
- https://cdn.elifesciences.org/articles/81405/elife-81405-supp1-v1.docx
