Skin cells of hagfish are capable of directly absorbing organic nutrients using specially adapted transport channels and leveraging sodium ion gradients.

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Absorbing nutrients from the environment is essential for all heterotrophic organisms. All but a few vertebrates accomplish this task by orally consuming food and absorbing freed nutrients through the gut epithelium. Nutrient uptake through the skin is not observed in most vertebrates because the skin, by nature, is meant to function as a tough, mostly impermeable barrier. However, Pacific hagfish have adapted to suit their feeding habitat by evolving the ability to absorb certain organic nutrients directly through their skin. Hagfish feed by burrowing through the decaying corpses of large animals, a rich stew of organic nutrients that have sunk to the ocean floor. In this environment, absorption of some nutrients through direct skin contact is a valuable adaptation. However, skin must also be a strong physical barrier and capable of denying passage of non-vital compounds. The hagfish solve this conflict by embedding active transport proteins in the skin epithelium cells. The transport channels are highly selective for specific nutrient substrates like amino acids. They derive the energy required for transport from a sodium ion gradient that exists between the outside of the skin cells and the inside. Like almost all cells, the hagfish actively pump sodium ions out of the cytoplasm. This creates a concentration gradient across the cell membrane. Allowing sodium ions to flow back into the cell through the transport channels fuels the energy-intensive uptake of useful nutrients (symport). Other factors like allosteric regulation can manipulate how compounds are absorbed through the skin. In this way, the hagfish permit the transport of select nutrients through an otherwise impermeable skin barrier.

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"Hagfish may feed by burrowing into decaying carcasses and eating their way out from the inside. This potentially exposes gills and skin to a nutrient-rich medium. Consequently, there is the opportunity for hagfish to absorb dissolved organic matter from the medium, similar to the scenario in estuarine invertebrates...This study showed, for the first time, the capacity for absorption of organic nutrients across a non-gastrointestinal epithelium in a vertebrate animal." (Glover et al. 2011:3096).

"The amino acids 3H-glycine and 3H-L-alanine were absorbed by both the gill and skin of the Pacific hagfish. Uptake profiles across each of these epithelia did not conform to typical hyperbolic concentration-dependent Michaelis-Menten kinetics, but instead best fitted sigmoidal distribution curves...uptake of glycine and L-alanine was sodium-dependent, with both showing a significantly reduced uptake in response to sodium substitution in the external medium." (Glover et al. 2011:3098).

"Gill and skin amino acid uptake may be a mechanism designed to maximize nutrient acquisition and represent an adaptation to a scavenging lifestyle...both substrates exhibited sodium dependence (indicative of sodium co-transport), mutually impacted the other’s absorption and displayed statistically indistinguishable kinetic uptake profiles. Co-transport with sodium is advantageous as animal cells maintain intracellular sodium at low levels to minimize perturbing effects on cellular components. This ensures that sodium influx into the cell is favoured and allows amino acids to use this electrochemical gradient to traverse the cell membrane...sodium dependence, nonlinear uptake kinetics and the modification of uptake by other amino acids strongly suggest that amino acid uptake in hagfish gill and skin occurs via specific transport pathways, rather than solely by diffusion." (Glover et al. 2011:3099).

"Given the large surface area of the skin it is clear that direct assimilation from the ambient medium could play a significant role in organic nutrient acquisition...It is important for hagfish to maximize the opportunity for nutrient acquisition when food is available. This appears to have been achieved, in part, by the capacity to absorb dissolved organic nutrients across their gill and skin, an ability not previously described in a vertebrate evolutionary trade-off between nutrient absorption and the need to limit exchanges across permeable surfaces." (Glover et al. 2011:3100).

Journal article
Adaptations to in situ feeding: novel nutrient acquisition pathways in an ancient vertebrateProceedings of the Royal Society B: Biological SciencesMarch 4, 2011
C. N. Glover, C. Bucking, C. M. Wood

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Pacific HagfishEptatretus stoutiiSpecies

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