Most fish breathe water with their gills, but a surprising number of fish can inhale air directly. Even common household pets such as Siamese fighting fish (betta fish, Betta splendens) breathe at the surface, so they can live in tiny bowls without filters or aeration. The Alaskan blackfish (Dallia pectoralis) shares this superpower. A modified esophagus lets them ‘surface breathe’, so they can get oxygen even in the stagnant and muddy waters that pepper the Arctic tundra. Most of the year, this ability gives blackfish a great advantage – they can live where most fish cannot, in a niche of their own. But in the winter, blackfish can no longer breathe air. The rough Alaskan winters bring ice and snow, which cover the water surface and lock out fresh air. Yet even after losing access to oxygen, blackfish remain active throughout the long winter season. For Gina Galli (University of Manchester, UK) and a team led by Jonathan Stecyk (University of Alaska Fairbanks, USA), this was a fascinating question. How can an animal survive for a whole season without air?To investigate, the team visited Palmer, Alaska, in the summer and caught blackfish with a minnow trap. Back in the lab, they housed the fish in aquaria and mimicked the conditions they would experience in the wild: over several weeks, they reduced the temperature to 5°C and reduced dissolved oxygen levels in the water. They also installed a grate just underneath the water surface to simulate the arrival of snow and stop the fish from breathing air. Then, they collected mitochondria – which are ideal to understand how oxygen is used, because they use oxygen to make energy – from the blackfish and analyzed how they were using oxygen. Do blackfish mitochondria work overtime to keep cells energized throughout the winter? It’s not unheard of, and Stecyk’s team noted that as many fish species acclimate to the cold, their mitochondria become more productive.But it turned out that cool temperatures did not energize blackfish. Their mitochondria didn’t fight any harder for oxygen. Likewise, they had the same appetite for a chemical needed to make energy (adenosine diphosphate, ADP), which means they weren’t making extra energy or working more efficiently. Unfazed, the blackfish mitochondria just chugged along at the same tempo.So, why don’t blackfish fight harder for oxygen? Stecyk’s team pointed out that although breathing sustains life, oxygen has a dark side. In any cell that consumes oxygen, a fraction of that oxygen creates toxic byproducts, called reactive oxygen species, which can damage mitochondria and kill cells. The researchers measured the reactive oxygen species produced by blackfish mitochondria using a fluorescent dye. In most species, cells produce more harmful reactive oxygen species when the temperature falls and oxygen is low – the exact conditions experienced by blackfish while breathless during Alaskan winters. Yet Stecyk’s team found the opposite: the blackfish produced fewer reactive oxygen species in the cold and fewer still when oxygen was low. This means the cold Alaskan winters prepare the blackfish to protect themselves from the damaging effects of low temperatures and oxygen levels, preconditioning them so they can hold their breath all season long.It’s fascinating enough that a fish can breathe air. But blackfish take it a step further: they hold their breath for an entire season. Many animals pant, gasp and struggle to get more oxygen when they can’t breathe, but blackfish don’t struggle. Their mitochondria maintain their pace, yet they work ‘cleaner’ to avoid polluting cells with toxic oxygen byproducts. In this way, they’re like a seasoned marathon runner: they don’t foolishly sprint when the race starts, they just maintain their pace and watch their form.
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