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Biology

The Secret’s in the Slime

Paper

Glover, C. N.; Blewett, T. A.; Wood, C. M. Novel route of toxicant exposure in an ancient extant vertebrate: Nickel uptake by hagfish skin and the modifying effects of slime. Environ. Sci. Technol. 2015, 49, 1896-1902. DOI: 10.1021/es5052815

The slimy hagfish: not your typical fish. (Source: phys.org/news/)

The slimy hagfish: not your typical fish. (Source: phys.org/news/)

Not Your Typical Fish

Hagfish are not your typical fish. In fact, it’s hard to believe that they’re fish at all. These long, slender boneless fish have no scales and produce slime to ward off predators. Hagfish are scavengers – they feed by burrowing into dead creatures on the sea floor. Researchers at McMaster University and University of Canterbury recently added to the list of the hagfish’s remarkably odd qualities: They discovered that the hagfish’s slime has other uses beyond defense; it also mediates uptake of toxins through the skin.

Not just with their mouths, but also with their skin and gills, hagfish feed by burrowing into carcasses of dead sea creatures. (Source: http://www.wired.com/2014/11/creature-feature-10-fun-facts-hagfish/ -- originally from Ryan Somma, Flickr

Not just with their mouths, but also with their skin and gills, hagfish feed by burrowing into carcasses of dead sea creatures. (Source: Wired Creature Feature — originally from Ryan Somma, Flickr)

Hagfish may be uniquely susceptible to toxic pollutants that accumulate in seafloor environments because they absorb nutrients through their skin and spend a lot of time burrowed into sediments or carcasses. Hagfish slime is a unique substance that has raised a lot of interest among researchers as a potential biomaterial, even bring proposed as an eco-friendly fabric. So, in addition to measuring uptake of metals into hagfish under normal conditions, researchers also wanted to investigate how this mysterious goo might affect the fish’s epidermal transport of metals.

The toxins under investigation were the metals nickel and zinc. Metals like these, often referred to as “trace metals”, are tricky toxins. They are essential nutrients for many living things and are no threat when present at natural levels. However, human activity has unearthed and displaced large amounts of metals, leading to higher-than-ordinary levels accumulating in some sediments and soils.

Methods

The researchers investigated the transport of metals and nutrients through hagfish skin by measuring accumulation of isotopically distinct analogs of each chemical of interest in hagfish in the laboratory. They caught wild hagfish and exposed them to water at three different nickel concentrations to determine whether uptake rates depended on the level of exposure and measured the accumulation metals in the hagfish’s skin and organs.

The authors compared uptake of two different metals – zinc, known to be utilized as a nutrient in trace amounts, and nickel, which does not have any known essential role as a nutrient for hagfish. They also measured uptake of an essential nutrient, the amino acid L-alanine, to determine whether the hagfish’s uptake of metals differs from uptake of typical ubiquitous organic nutrients.

To determine whether the hagfish’s slime had any effect on uptake of metals, the researchers took slime secreted by one hagfish and smeared it on samples of hagfish skin, then compared uptake of metals and nutrients into this skin to uptake in non-slimy hagfish skin.

Results

(i) More nickel in the water means more nickel in the fish

Regardless of the nickel concentration that hagfish were exposed to, the majority of the nickel (~ 93-98%) accumulated in the skin, whereas very little continued traveling through the skin and into organ systems. As you might expect, hagfish exposed to higher levels of metals in the water ended up accumulating higher levels in their bodies.

(ii) Nickel ends up in unexpected organs

Most of the nickel that passed through the skin was found in the gills, brain, and heart. High concentrations in the gills suggest that gill uptake is a significant exposure route for hagfish, along with skin uptake, though the relative importance of the two pathways is not known. The authors state that accumulation in the brain and heart suggests that nickel might have some biological use in hagfish, perhaps as a trace level nutrient, but this has not been confirmed.

Nickel accumulation measured in different body compartments after exposure of hagfish to 10 uM nickel concentration. At all three exposure concentrations, the highest concentrations of nickel were measured in the gill, heart, and brain.

Figure 1: Nickel accumulation measured in different body compartments after exposure of hagfish to 10 uM nickel concentration. At all three exposure concentrations, the highest concentrations of nickel were measured in the gill, heart, and brain.

 (iii) Slime on the skin modulates metal transfer

Interestingly, the researchers found that slime application had a significant effect on transport of metals through hagfish skin. At low concentrations of metals, the added slime significantly reduced the uptake rate of zinc and nickel into the skin, though it didn’t affect uptake of the amino acid L-alanine. Their results suggest that nickel binds to a chelating agent in the slime – some unknown compound that forms multiple bonds to the metal and immobilizes it. At higher water concentrations, the authors posit that the chelating agent becomes saturated. Once all of the chelating agent is bound to metals, it can no longer impede uptake of the metal, and the slime stops having a significant effect on metal uptake.

Black columns show the uptake rate of nickel and zinc through hagfish skin. White columns show the uptake rate on slime-treated skin. In the top plot (low metal level exposure there is a pronounced decrease in metal uptake after slime is added to the skin, but the same decrease is not seen in the bottom plot (higher metal level exposure).

Figure 2: Black columns show the uptake rate of nickel and zinc through hagfish skin. White columns show the uptake rate on slime-treated skin. In the top plot (low metal level exposure there is a pronounced decrease in metal uptake after slime is added to the skin, but the same decrease is not seen in the bottom plot (higher metal level exposure).

Significance

This study suggests that the hagfish’s slime acts as a “selective filter” that impedes passage of trace metals that could cause toxicity at high levels, but allows transport of large organic molecules like amino acids. The authors note that further research is needed to determine whether other large organic molecules like persistent organic pollutants are transferred similarly to nutrients.

The accumulation of metals at toxic levels in hagfish could affect humans, as hagfish are featured in the cuisine of some cultures. The accumulation of toxins in hagfish could also negatively impact their populations, which could perturb sea floor ecosystems in which hagfish play an important role. As scavengers, hagfish remobilize organic matter that has fallen to the seafloor, bringing it back into the food chain and providing a valuable food source to predators in an environment where there is little food available.

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