June 2010

Artificially colored satellite image of the Arctic region; an area that consists of a vast, ice-covered ocean surrounded by treeless permafrost. In recent years the extent of the sea ice has declined because of climate change. Photo: Screenshot from NASA’s globe software World Wind.

What makes sea ice interesting?

Deming: Sea ice is fundamentally different from freshwater ice. It contains salt because it forms from seawater. That salt depresses the freezing point, so seawater can remain in liquid form at colder temperatures than is possible for freshwater. So, some liquid remains inside of sea ice as it forms, making it a porous habitat where microorganisms can survive and even thrive. You will not find such microbial activity in glacial ice because glacial ice is derived from freshwater (from snow). There are only tiny amounts of liquid water in glacial ice, not enough for significant reproductive activity or growth to go forward.

What makes Arctic sea ice so interesting to study is that, in winter, it can get colder than any other saline ice formation on the planet yet still contain liquid habitats. In contrast, sea ice in the southern ocean surrounding Antarctica is mainly seasonal, experiencing milder winter conditions than in the high Arctic. The Antarctic continent itself experiences colder temperatures than the Arctic, but freshwater glacial ice covers Antarctica, not salty ice.

How do organisms survive in the coldest ice??

Deming: Warm summer ice in the Arctic—by warm I mean -2° instead of -20° or even colder as you would find in the wintertime—harbors photosynthetic life (sea-ice algae) and more complex multicellular life (protozoa, nematodes, and crustaceans) that are active as long as the ice is warm enough. However, I am interested in what happens in the coldest ice that still has enough liquid water in it to support active microbial life forms and so I go to the Arctic in the winter.

This natural-color image shows winter ice hugging the coastline of Canada’s Baffin Island in the Arctic Circle. Photo: July 2009, NASA Earth Observatory.

There I study the phylogenetic domains of Bacteria and Archaea—single-celled microorganisms that are typically not more than a micrometer in length. You would need a microscope that magnifies many thousandfold to see one of these little creatures. Even though both of these domains contain only single-celled microbes that often look very similar under the microscope, they are completely different from each other genetically. Bacteria have long been known to live in sea ice in all seasons, but Archaea, best known for their “extremophile” lifestyles, have only recently been discovered (by my former graduate students Karen Junge and Eric Collins) in sea ice and so far only in Arctic winter sea ice.

In my lab, although we work mainly on Bacteria and Archaea, we have also done some work on ice algae. This ice algal work led to the discovery of what we call extracellular polysaccharide substances (EPS), which consist of complex sugar compounds that are released by an organism into its surroundings. Ice algae release a lot of this gelatinous material when they are photosynthesizing and fixing carbon, and especially if they come under environmental stress. We believe that these EPS further depress the freezing point (like salt) and keep the pore spaces within the ice filled with at least some liquid (called brine) through the winter rather than freezing up entirely.

The discovery that ice algae have the ability to maintain a liquid environment in sea ice was made by a former postdoctoral associate, Christopher Krembs. He brought this discovery to my lab where we have translated it into our work with Bacteria and Archaea. We have found that ice-adapted bacteria can also produce copious amounts of EPS. Even if they find themslves in very dark cold winter ice—with no ice algae around to produce this gelatinous material for them—they can produce it on their own. It’s an amazing mechanism for controlling your immediate environment in ice and surviving extreme conditions as a result.

Are microbes producing this EPS for insulation?

Deming: Insulation is a good word for starters. EPS provide insulation or a kind of buffer against two conditions: subfreezing temperature and high salt content. We think EPS act as natural antifreeze against the temperature as it drops in wintertime—by that I mean that it depresses the freezing point a bit further than does salt alone so that the immediate surroundings of the cell remain liquid, even below -20°C. In other words, ice crystals cannot form near the cell and cause freeze-damage by puncturing a membrane or cell wall.

The other role that EPS can play is to provide a buffer against salt. When an organism in sea ice is in one of those interior pores that still contains liquid in wintertime, this liquid will also contain a lot of salt. We can see microscopically that EPS provide coatings that surround the microbial cells in those sea-ice pores. These EPS gels are what we call hydrated—they can have more water within them than in the surrounding brine. We think that a microbe is surrounded with enough of this watery, mucous-like material to be physically buffered against the high-salt brine that is just beyond its sugary coating. We think, therefore, that an EPS coating simultaneously protects a cell against ice damage and high salt concentrations.

When did sea ice microbes evolve this survival mechanism?

Magnified view of brine channels in Arctic sea ice. EPS alters the structure of sea ice pores. Photo: Christopher Krembs and Jody Deming.

Deming: We know that many sea ice organisms carry genes that allow them to produce EPS material that protects against freezing and osmotic shock. This material provides cryoprotection against freezing and osmoprotection against salt shock, both of which happen to any organism that goes through a freeze-thaw cycle in seasonal sea ice and that experiences shifts from freshwater to saltwater or from saltwater to freshwater. We know that both ice algae and bacteria produce EPS material and, though we do not know for sure yet, we suspect that at least some archaea produce EPS. There are also examples of more highly evolved fauna that live in ice that also coat themselves up with sugary mucous-like material. It seems to be a common strategy for living and surviving in sea ice.

As for dating the evolution of this trait, geologically or phylogenetically, this is the question we wish we could answer. Researchers can date geologically the timing of the last glacial period and those before it, for Earth has gone through a series of glacial and interglacial periods. Between the glacial periods, the habitat of ice no longer existed. The cold-adapted microbes either had to re-evolve with each glacial period or find some refuge when the Earth became too warm to support ice. I think this refuge may have been the cold deep sea. Organisms that evolved in ice may have found a way to survive in the cold deep sea, while the surface of the earth was still too warm for ice.

If they had to “re-evolve,” however, then sea ice may have provided the environmental setting for that process to occur. Winter sea ice, in particular, is a unique environment for the way in which it concentrates bacteria, archaea, and viruses together in very high densities within the small, interior pore spaces of the very cold ice. By virtue of packing many microbes and viruses together in a small space, the predatory viruses have greater access to their potential microbial hosts than they would if they were free-floating in diluted seawater. So the contact rate is much higher—600 times higher than it is in seawater (based on model calculations by one of my former graduate students, Llyd Wells), and that sets up the potential for “horizontal,” also called “lateral,” gene transfer [when an organism incorporates genetic material from another alien organism, in this case transmitted via viruses]. This high contact rate also sets up the potential for the virus to attack the cell, reproduce within it, and then cause cell lysis [death of a cell when its contents spill out after a break in the cellular membrane]. There is evidence for both virus-mediated cell lysis and gene transfer in ice-adapted bacteria.

The evidence for lateral gene transfer comes from the available whole genome sequences of cold-loving and ice-dwelling bacteria. All of those genomes contain genes that appear to have been delivered to them by viruses. By the way, chemicals like calcium ions that are needed in a laboratory experiment to promote horizontal gene transfer by viruses are readily available naturally in sea ice. The habitat, therefore, appears designed to encourage this process to happen. We think it may help the evolutionary process move forward even in the face of the extreme conditions of very low temperatures and high salt concentrations.

Why a high ratio of viruses to bacteria when the sea ice habitat is such a small, closed space?

Deming: Well, in seawater, you typically have a ratio of 10 to 1 viruses to bacteria because of the burst of viruses that comes out of a lysing bacterium. Those viruses have a variable lifespan—their decay rate depends on their environment, which is another interesting aspect of sea ice. Their decay rate in sea ice is so slow as to be difficult to measure. They are able to survive as long as we have monitored them. We’ve examined them periodically for weeks on end under sea-ice conditions, and they are still there visibly (microscopically) and still functional, able to infect bacterial hosts. In contrast, in seawater, at say 4 to 15°C, their decay rates are pretty rapid—on the order of hours or days, but usually hours. So one reason we may have such high concentrations of viruses in sea ice is because they are not dying off, they are able to persist in the very cold conditions.

A field of frost flowers in the high Arctic. These flowerlike ice crystals grow on newly formed ice. The “petals” of these frost flowers are about one centimeter in length. Photo: Eric Collins.

What is your newest sea ice project?

Deming: I am very excited about our new work with frost flowers, which are delicate ice crystal structures that literally look like flowers. They appear on the surface of newly formed sea ice in both the Arctic and the Antarctic. We discovered last year that they contain elevated concentrations of bacteria and bacterial viruses—higher than in the sea ice on which they grow, so we are very eager to ask the question: Are these organisms active?

One of the reasons that this discovery is so exciting to us is because frost flowers usually form at a very cold temperature—the air has to be at least -8°C for them to form at all, but is often -20° or colder. We have managed to grow frost flowers in a freezer laboratory set to -26°C so far, but they form in nature at -30° and even colder. So this newly discovered habitat is even colder than the sea ice they grow on, allowing us to ask new questions about the lower temperature limit for active life.

Also let me say that we have not demonstrated yet that the viruses and the bacteria travel in the same numbers into frost flowers. We have some preliminary data to suggest that is the case. With recent funding by the National Science Foundation, we will use our freezer-laboratory system to grow frost flowers, starting with a known number of viruses and a known number of bacteria and literally watch them move upwards into the growing frost flowers and then, hopefully, determine if they are interacting under extreme conditions.

How is your research useful to studying life beyond Earth?

Model of Europa’s interior showing a solid ice crust over a layer of liquid water or soft ice, a silicate mantle and a metallic core. Europa, one of the six moons of the planet Jupiter, is slightly smaller than Earth’s Moon. It was discovered in 1610 by Galileo. Source: NASA photojournal.

Deming: I was terribly motivated by the discovery of a possible and now very likely, very large ocean on Europa—a moon to Jupiter; this discovery inspired me to shift gears in my research plans. I had been working in the deep sea before, but I quickly developed a new focus on ocean surface waters that freeze, leading to extremely cold and salty ice environments.

The idea of an ice-covered ocean elsewhere in our Solar System has always fascinated me. I believe my students and I can transcribe our adventures of learning about how microbial life has adapted to very cold ice on Earth to other solar bodies. Research questions such as “What is the lower temperature limit for life as we know it?” have been asked in studies on Earth, but the answers can also be applied beyond Earth. Scientific knowledge of the temperature limits for various life processes could help NASA [National Aeronautics and Space Administration] decide where they would land a spacecraft on Mars, for example. Do they need to go to an ice-capped region? Do they need to sample where there might be enough of a temperature gradient that you could expect to find some porous ice in the subsurface with liquid-filled spaces similar to Arctic sea ice?

Does science have an answer to “What would be the temperature boundaries for life as we know it?”?

Deming: One of my former students, Karen Junge, produced thesis work showing that the lower limit for activity fell below -20°C. She did that work in the early part of the 2000s and the results of her work were published in 2004. NASA still uses this temperature as the lower limit for Earth life to remain active on Mars (from the planetary protection perspective). To be cautious in their planning, NASA has set the limit down to -25° until more data are forthcoming; but, we feel we have already helped by establishing today’s lower temperature limit for active microbial life.

Before this work, the lowest temperature for microbial activity was warmer. Over years of work, researchers have been adjusting the limit gradually, first from 0 to -5°C, then to -10 and -15°C. Now it has been pushed to -20°, and we continue to search for evidence that will push it even lower. I think one of the reasons that the scientific community has been cautious in these estimates in the past is that we have lacked imagination or motivation to even ask the big question: Is it possible for life to exist and evolve under even more extreme conditions than we have on Earth? With the recent discoveries of colder ice-covered oceans and moons elsewhere in our solar system, we now have ample motivation.

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