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Physiology

Icefish can’t keep their cool in warm water

Almroth, B.C., Asker, N., Wassmur, B., Rosengren, M., Jutfelt, F., Gräns, A., Sundell, K., Axelsson, M., & Sturve, J. (2015). Warmer water temperature results in oxidative damage in an Antarctic fish, the bald notothen. J. Exp. Mar. Biol. 468: 130-137.

Fig. 1. The bald notothen (Pagothenia borchgrevinki) lives in the Southern Ocean, and is often found just beneath the ice, foraging for prey items like copepods and krill.

Fig. 1. The bald notothen (Pagothenia borchgrevinki) lives in the Southern Ocean, and is often found just beneath the ice, foraging for prey items like copepods and krill. Image: Google

The Antarctic is the premier example of a cold, strange, and desolate place (even for Canadians like me). Well, it’s not that desolate. Quite a few marine organisms make their living among glaciers and beneath the sea ice, including icefishes like the bald notothen (Pagothenia borchgrevinki). Icefishes are a diverse group that thrives in the frigid Southern Ocean due some unusual physiology: their blood is similar to antifreeze, they have large numbers of energy-supplying cellular structures called mitochondria, and their body and skeletal densities differ from most temperate species. Unfortunately, some of the unique adaptations of icefish also make them extremely susceptible to the effects of global warming.

Cold, but getting warmer

And, increasingly, large sections of Antarctica are not that cold, at least compared to the historical data. At the forefront of climate change, the average surface temperature of the continent has increased over 0.05°C per decade since 1957, particularly in the Western end (Steig et al., 2009). For icefish, which have lived for 10-15 million years within a narrow temperature margin (-0.5 to -1.9°C, 29 to 31°F), this is a rapid and substantial environmental shift. As the ecosystem’s most abundant fish taxa, how effectively icefish are able to adjust (or not) to warming temperatures will have a huge impact on the future biological health of the region.

Warm water means oxidative stress

Fig. 2. Icefish were angled from the sea ice at Evans Wall, Ross Island, McMurdo Sound, Antarctica, before being transported to the Crary Lab at the McMurdo Sound Station (pictured here) for experiments.

Fig. 2. Icefish were angled from the sea ice at Evans Wall, Ross Island, McMurdo Sound, Antarctica, before being transported to the Crary Lab at the McMurdo Sound Station (pictured here) for experiments. Image: Google

For cold-blooded icefish, for which body temperature is determined by the animal’s environment, even slight changes in water temperature have serious consequences. Adding heat increases the speed of all the chemical reactions involved in biological process like growth, digestion, and respiration – think of how you can bake cookies in the oven at 400°F, but not on the kitchen table at room temperature. So, putting an icefish in warm water immediately increases both their metabolic rate (the sum of all the chemical reactions occurring in a living organism) and the production of any by-products of cellular metabolism, like reactive oxygen species (ROS).

 

The problem with ROS is their instability, meaning they interact unpredictably and easily with all sorts of cellular components. These interactions cause damage to the cell by deactivating or even changing the function of important structures like proteins and cell membranes (Fig. 3). This sort of oxidative damage in humans has been implicated in aging, and in a host of health problems like sleep apnea, cancer, and some cardiovascular diseases.

Fig. 3. Reactive oxygen species (ROS) are a by-product of energy production in the mitochondrion, and can damage cellular structures. ROS levels are tightly controlled in the cell by antioxidant molecules and antioxidant enzymes like superoxide dismutase and catalase. Left unchecked, ROS can damage important cellular structures like proteins, DNA, and membranes. Borowiec, 2015.

Fig. 3. Reactive oxygen species (ROS) are a by-product of energy production in the mitochondrion, and can damage cellular structures. ROS levels are tightly controlled in the cell by antioxidant molecules and antioxidant enzymes like superoxide dismutase and catalase. Left unchecked, ROS can damage important cellular structures like proteins, DNA, and membranes. Image: Borowiec, 2015.

Now, oxygen-dependent metabolism has existed for a long time, and organisms have evolved defense mechanisms to minimize the oxidative damage caused by ROS (Fig. 3). Antioxidant molecules (vitamins C and E, glutathione, melatonin, others) soak up excess ROS by binding to them before they reach more sensitive cellular structures. Similarly, there are antioxidant enzymes that are able to safely react with ROS and convert them into less damaging forms. A good defense system can minimize the effects of large increased in ROS production.

Icefish are vulnerable to oxidative stress

Fig. 4. Icefish are more vulnerable to heat-induced oxidative stress. Their relatively unsaturated (fluid) cellular membranes are more vulnerable to oxidative damage than the membranes of temperate species. Icefish also have a high density of mitochondria, which are the major producers of ROS in the cell. Image: Borowiec, 2015.

The physiology of Antarctic icefish makes them particularly vulnerable to oxidative stress brought upon by an increase in water temperature (Fig. 4). To survive in the cold Southern Ocean, these animals have evolved a high density of mitochondria (major producers of ROS), and have a lot of unsaturated fats in their cellular membranes (which are more vulnerable to oxidative damage than saturated fats). This means icefish are in the precarious position of having both more sites where ROS can be produced, and membranes that are more easily damaged by ROS.

To test the hypothesis that icefish were extra susceptible to oxidative damage, and the potential consequences of this vulnerability, Almroth et al. acclimated icefish to acute (short-term, 12 h) or chronic (long-term, 3 weeks) elevations in water temperature (4°C), representing a hypothetical future heat spell, and then compared their antioxidant defense mechanisms.

Warm water acclimation in icefish

Fig. 5. Activities of enzymes involved in antioxidant defense in icefish exposed to short-term (“acute,” red) and long-term (orange) elevations in water temperature, relative to animals at a cooler, typical water temperature (“control,” blue). Higher enzymatic activity (vertical axis) suggests a greater capacity to deal with reactive oxygen species (ROS). Bars denoted by the same letter are not significantly different from each other. Enzymes are abbreviated as follows: SOD, superoxide dismutase; CAT, catalase; GR, glutathionine reductase; GPX, glutathionine peroxidase; GST, glutathionine S-transferase; G6PDH, glucose-6-phosphate dehydrogenase. Adapted from Almroth et al., 2015.

Fig. 5. Activities of enzymes involved in antioxidant defense in icefish exposed to short-term (“acute,” red) and long-term (orange) elevations in water temperature, relative to animals at a cooler, typical water temperature (“control,” blue). Higher enzymatic activity (vertical axis) suggests a greater capacity to deal with reactive oxygen species (ROS). Bars denoted by the same letter are not significantly different from each other. Enzymes are abbreviated as follows: SOD, superoxide dismutase; CAT, catalase; GR, glutathionine reductase; GPX, glutathionine peroxidase; GST, glutathionine S-transferase; G6PDH, glucose-6-phosphate dehydrogenase. Image: Almroth et al., 2015.

Acute (12 h) exposure to 4°C increased antioxidant defenses in icefish, and this was due to increases in both the gene expression and activity of some antioxidant enzymes (Fig. 5). This contrasts with some earlier work that suggesting that the bald notothen was unable to respond to acute temperature stress. Instead, it appears that the species responds like most temperate fishes in spite of its narrow (and specialized) preferred temperature range.

Fig. 6. The livers of icefish exposed to long-term, but not short-term (“acute,” red) elevations in water temperature had increased levels of oxidative damage to both proteins (A) and fats (B) relative to control animals (blue). Bars denoted by the same letter are not significantly different from each other. Adapted from Almroth et al., 2015.

Fig. 6. The livers of icefish exposed to long-term (orange), but not short-term (“acute,” red) elevations in water temperature had increased levels of oxidative damage to both proteins (A) and fats (B) relative to control animals (blue). Bars denoted by the same letter are not significantly different from each other. Image: Almroth et al., 2015.

Interestingly, long-term (3 weeks) exposure to the same temperature had a much less dramatic effect than the acute exposure, such that more antioxidant genes and most antioxidant enzymes were similar to control levels. Moreover, animals exposed to long-term elevations in water temperature also had higher levels of oxidative damage to both proteins and fats (Fig. 6), indicating that their antioxidant defenses were not sufficient to prevent damage. This suggests that a prolonged increase in ocean temperature may result in an increased rate of physiological aging in this species, and loss of function and fitness.

Climate change in the Antarctic

The polar regions are among the most vulnerable to climate change, meaning many of their inhabitants are facing unprecedented shifts in their environment. Due to their narrow temperature ranges and some unique adaptations for Antarctic life, icefish seem to have an innate physiological sensitivity to the oxidative stress induced by exposure to increased temperatures. As the dominant fish taxa in a fragile ecosystem, icefish fill a variety of niches and are a key, intermediate component of the Southern Ocean’s food chain. As global climate change marches on, further work needs to be done to appreciate its full effect on the polar environment and the animals that inhabit it.

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