groundhog head peeking up between two branchesIt’s February, often Dayton’s coldest month. Groundhogs, aka woodchucks, which amuse us with their antics during the warmer seasons, have long since hidden away in their underground hibernation retreats. At the same time, the broad green leaves of skunk cabbages, which mark the wet woods and marshes of summer, have died off, leaving their copious root systems to survive until the next growing season.

So, what do these two seemingly unrelated organisms, one a mammal and one a plant, have in common? The whole-organism answer is that neither of them waits for warm weather to “wake up.” Rather, both groundhogs and skunk cabbages initiate activity while the mercury sits low in the thermometer. It also turns out that groundhogs and skunk cabbages share a deeper commonality. That is, they both warm themselves against the cold using a protein shared from deep evolutionary history.

Groundhogs are among the largest true hibernators, meaning those mammals whose body temperature drops substantially for an extended period. (Bears do spend the winter in lethargic slumber, but their body temperature drops by just a few degrees.) Groundhog body temperature drops from 36oC (97oF) to about 10oC (50oF) during hibernation. At the same time, bodily functions slow profoundly. Heart rate, for example, drops from ~80 to ~5 bt/min, and breathing slows to just a couple of breaths per minute. The marked decrease in cellular metabolism at low body temperature means that the animal can survive for several months on nothing but the energy reserves (mostly fat) that it accumulated during the previous fall.

Despite all that, groundhogs, like other mammalian hibernators, don’t remain at uninterrupted low body temperature throughout their nearly five months of hibernation. Rather, every 6 days or so they arouse for about 1.5 days. (Needless to say, most groundhogs don’t time an arousal to fall on February 2 each year–Punxsutawney Phil notwithstanding.) During those arousals, body temperature temporarily rewarms to normal before cooling back to hibernation levels. Arousals can account for more than 90% of all energy use during hibernation, and their exact function remains unclear. They might allow the animal to urinate and thereby rid its body of accumulating wastes, or they may allow sensing and synchronization with environmental cues.

The rise in body temperature during arousal from hibernation is rapid, and it is achieved not by shivering but through the activity of a specialized tissue called brown fat. Brown fat is characteristic of hibernators, in which it is localized most prominently between the shoulders. It’s present in infants of some non-hibernators, too, including humans, but tends to disappear by adulthood. Brown fat has one specific function: to generate heat. The process is called “non-shivering thermogenesis,” and the key is a molecule called uncoupling protein, or UCP1. In mammals, UCP1 is active only in cells of brown fat. Within those cells, UCP1 sits in the inner membrane of the mitochondria (mitochondria have a double membrane, inner and outer). Those organelles are known as the powerhouses of the cell because they synthesize ATP, which stores cellular energy. The process that drives ATP formation in the mitochondria involves an enzyme (ATP synthase) that is powered by the movement of hydrogen ions (protons) across the mitochondrial inner membrane. It’s analogous to water generating electricity by flowing through a dam’s turbine.

That’s where UCP1 comes in. UCP1 “uncouples” the movement of hydrogen ions from the action of ATP synthase. Instead of powering ATP synthase, the energy from the hydrogen ion movement is dissipated as heat. (To pursue the analogy, it’s as though the turbines were bypassed and the water was allowed to just flow downstream, without producing electricity.) The result is that brown fat doesn’t produce a lot of ATP, but it does produce a lot of heat.

It turns out that skunk cabbages use exactly the same trick. Skunk cabbage is famously among the earliest plants to emerge from winter, often appearing as early as late February. And it accomplishes that by using the amazing trick of melting its way up through the snow. In particular, the spadix of the plant (the central spike that eventually will support the plant’s tiny flowers) heats up as it grows. And that heat is generated in just the same way as occurs in brown fat, a function of UCP1 acting in the mitochondria of spadix cells. As a result, the spadix can keep its internal temperature at ~20oC (68oF), even in air temperatures below freezing.

How did two organisms as unrelated as a swamp-dwelling plant and a woodland mammal both end up having the same protein? It now appears that uncoupling proteins probably arose quite early in evolution. Even some single-celled organisms like amoebae possess genes that code for UCP-related molecules. That’s really not too surprising. One of the key lines of evidence supporting the deep relatedness of all living things, from bacteria to fungi, plants, and mammals, is that they share so much molecular machinery, including DNA, ATP, and many other examples. Useful molecules that arise in evolution persist, sometimes retaining their original function, sometimes modified or co-opted for other uses. Amoebas appeared in evolutionary history something like a billion years ago, and so there has been lots of time for those molecules to diversify. UCP1 from plants (skunk cabbage) and from mammals (groundhogs) have diverged somewhat over time, the result of mutations coupled with the demands of living in particular environments. But they are on the same branch of the UCP family tree and they retain the same basic structure and function. On the other hand, UCP1 is just one of several related proteins in the UCP family. Mammals, for example, have several versions (UCP2, UCP3, and others) that are active in various tissues and that may have a variety of functions, like as anti-oxidants.

As Punxsutawney Phil emerges to check for his shadow one state to our east, our local groundhogs and skunk cabbages also will be mobilizing to meet the cold. UCP1 will be doing its thing and, from the depths of underground, and of time, the first signs of spring warming will arise.

Article and photo contributed by Dr. David L. Goldstein, Emeritus Professor, Department of Biological Sciences, Wright State University.