Microbes have long done the world's dirty work. They gobble up oil spills. They defend our guts against disease. And even in rugged northern latitudes, hosts of bacteria filter through the soil, feeding on falling leaves and decay, freeing carbon and nutrients for each spring's renewal.
For a long time, scientists thought the essential role played by soil bacteria in the northern carbon cycle was purely seasonal: During summer, heat-loving bugs would tear through leaf litter and waste with a frenzy, multiplying rapidly. Then, as winter's cloak descended and dirt froze, the microbes would act as microscopic bears, barely alive, waiting for the thaw.
"We assumed that things in the freezer were frozen," said Josh Schimel, an environmental scientist at the University of California, Santa Barbara. "There was this idea of 'last one out, turn off the lights,' that Arctic systems just shut down."
But scientists have discovered in recent years that the carbon cycle never sleeps for soil bacteria. Using trapped pockets of salty water and creating their own antifreeze, bugs are stubborn survivalists. Up to a third of yearly CO2 emissions from northern soils can occur in winter, driven by microbes. And recent research has found that not only are these bugs surviving. They're getting busy.
Two recent studies in particular have overturned previous notions that bacteria in frozen soils focus all their energy on surviving cold stresses. Work by Schimel, along with a study published this month by Swedish scientists, has instead found that even at several degrees below freezing, soil bacteria are dividing and reproducing, often at rates equal to warmer-weather processes.
The findings add to a growing body of evidence that frozen soils, long known to store vast reserves of ancient carbon, could be more sensitive to warming than previously understood. While it is risky to extrapolate any one finding to the broader climate, especially in soil -- where all bacteria are local -- the studies indicate that frozen permafrosts could be well-adapted to release CO2 under a bit of warming, said Mats Oquist, a forest scientist at the Swedish University of Agricultural Sciences.
"It is likely that microbes in permafrost are quite viable and adapted to the frozen environment, as we saw in our study," Oquist said. He is eager to apply his techniques, detailed in a paper earlier this month in the Proceedings of the National Academy of Sciences, to tundra and other permafrost, he said, "since a lot of soil carbon is stored in these areas."
Oquist's study and other recent soil work raise important questions about how carbon models are constructed, added Ben Bond-Lamberty, a scientist at the Joint Global Change Research Institute at the University of Maryland.
"These microbes are doing a lot more than staying alive," Bond-Lamberty said. "And as we construct annual carbon budgets, this raises the possibility that there's a lot more wintertime CO2 coming out of these systems than we realized."
Little known about frozen soils
Estimates vary on the exact amount of carbon sequestered in the permafrost, though all agree it is massive; one recent attempt, compiled by a consortium of soil scientists, tagged it at double current atmospheric CO2 levels. And while much of that carbon would only decompose at sustained temperatures above freezing, it is clear that a move from even negative 8 to negative 4 degrees Celsius will spur some decomposition, said Ted Schuur, a permafrost expert and ecologist at the University of Florida.
"The threshold is a few degrees below zero," Schuur said.
Schuur's current research, though unpublished, has found that not all carbon stored in permafrost is created equal and will resist broad characterization. But from samples he has taken, it appears that under thawed conditions, between 40 and 70 percent of the carbon stored in permafrost would escape to the atmosphere within a decade, a rate far faster than spreading vegetation can absorb.
"Something like plant growth won't be able to offset it on that time scale," he said.
Overall, the world's annual soil respiration -- the flux of CO2 released by microbes and then absorbed by plants -- remains poorly understood. But over the past few decades the overall rate of CO2 released into the atmosphere has accelerated, according to work published this year by Bond-Lamberty in Nature.
Along with a colleague, Bond-Lamberty assembled more than 400 studies of soil respiration from the past half-century. Using sophisticated statistical methods, they found that CO2 respiration seemed to be increasing at a rate matching the rise in global temperatures over the past two decades. It was not a surprising result, since microbes tend to flourish under higher temperatures, and it remains uncertain whether increases in plant life have compensated for the increase microbial activity.
While compiling his survey, Bond-Lamberty found very few studies of northern soils to include in his analysis, and the records he did find -- and the conflicting signals he derived from them -- suggested scientists know very little about northern soils.
"There's a lot of carbon there," he said. "And we don't have a good handle on what's going on."
Frozen soils have remained an enigma for many human reasons. Monitoring soil bacteria in frozen samples is a challenge, and only recently have scientific tools eased the process. Also, it is not a pleasant trip to chop out soil specimens in northern Canada, Alaska or Siberia. Instead scientists would study the soil in the summer and assumed that deep freezes slowed everything down to a halt.
It is an intuitive, downright seductive idea, Santa Barbara's Schimel said.
"Things are rough," Schimel said. "They don't have [great] access to resources. ... It might be so stressful that they would maintain metabolic activity, not actually thriving and growing. Just toughing it out."
'Bacteria don't read textbooks'
Earlier this decade, though, scientists like Jeffrey Welker at the University of Alaska, Anchorage, started measuring CO2 in winter snow packs.
The gas was accumulating, they found, suggesting biological activity. Before then, some flawed Russian studies had hinted at activity, but only in the past few years has enough science accumulated to begin to revise expectations for frozen soil life.
Scientists were primed to discover the bacteria because, even in the most extreme cold, it was becoming apparent how well microbes could get along. Scientists had found microbes happily living at temperatures 39 degrees below zero, Schuur said. They were in soil overridden by glaciers. They were in cloud droplets, and in bone-chilling fringes of the deep sea. They were even in ice cores.
With this in mind, Oquist and his colleagues surmised that the CO2 they were seeing released from frozen soils reflected more than just bacteria riding out the cold snap, he said. If bacteria were growing in ice cores, why not beneath Sweden's snowpack?
The researchers devised an elegant method to test their theory. Beneath spruce eaves in northern Sweden, they carved out soil samples, which they then stored at 20 degrees below freezing. The sieved soils were then fed simple sugars assembled with a radioactive isotope of carbon and allowed to stew at temperatures above and below zero for several months in the lab.
Every so often, Oquist scanned the soils using nuclear imaging, which revealed how the bacteria had, or had not, digested the tagged sugars. (The scans helped the scientists overcome a traditional limitation in their field: how to sample soil while keeping it frozen.) There was little activity at negative 9 degrees Celsius, they found, but at negative 4 degrees, a majority of the sugar had been used up.
The CO2 emitted by these bacteria was only a small share of the consumed carbon, some 14 percent. Most of it went instead toward building out the fats, proteins and other building blocks needed for reproduction. The bacteria even increased their production of glycerol -- a type of antifreeze.
"These microbes are basically using antifreeze to stay active," Florida's Schuur said.
While Oquist's study -- along with work published by Schimel last year -- seems to confirm that bacteria can thrive in frozen soil, this needs to be tested more in the wild, Schuur added. The Swedes used a simple sugar to feed their bacteria, while up north, ancient, complex carbon is stored in soils. It is uncertain whether bacteria will be able to use such complex molecules as easily, he said.
Another uncertainty is whether different varieties of bacteria take over once a soil drops below freezing, or whether the bugs adapt, Schimel said. He has graduate students trying to do mass analyses of the proteins and DNA found in frozen soil but that "kind of work is really, really hard," he said. "Soil is dirty. Microbes are diverse. Analyzing their in-situ physiology is a bear."
"Bacteria don't read textbooks," he added. "They don't always do what we think they're supposed to do."