Life in Extreme Environments: The Universe May Be More Habitable Than We Thought: Part 2

Continued from PART 1

Note: A shorter version of this article appeared in the May/June 2002 issue of the National Space Society's Magazine Ad Astra. Reprinted here with the author's permission


Evaporation pond in Baja, Mexico. The red color is due to carotenoid pigments released by halophilic (salt loving) bacteria.
Salinity

As airplanes descend into the San Francisco area, red patches on the eastern shore of the South Bay are conspicuous. These are evaporation ponds of Cargill Salt Company. The cause of the red color is halophilic (salt-loving) microbes that produce red pigments called carotenoids. A similar situation occurs in salt flats, such as the Great Salt Lake in Utah, and deep sea hypersaline basins. The microbes involved are either members of the Archaea, a major group of microbes superficially similar to bacteria, or the green alga Dunaliella salina. At a bit lower (25-33% ) salinity, bacteria, cyanobacteria, other green algae, diatoms and protozoa are found. Some Archaea, cyanobacteria, and Dunaliella salina can even survive periods in saturated sodium chloride - about as salty an environment as one can imagine.

Salt water can evaporate leaving deposits ("evaporite deposits") consisting of salts such as sodium chloride (halite) and calcium sulfate (gypsum). Within evaporates are fluid inclusions - small trapped pockets of water - which can provide a refuge for microbes for at least six months. Our research group showed that cyanobacteria trapped within dry evaporite crusts can continue to have low levels of metabolic function such as photosynthesis. These deposits also form nice fossils of the organisms trapped within. Although highly controversial, others claim that bacteria might survive for millions of years in the fluid inclusions of salt deposits including evaporates. Tantalizingly, such deposits have been found on Mars.

So how do cells adapt to this potentially deadly environment? To prevent an exodus of water from the cell, halophiles offset the high salt in the environment by accumulating such compounds as potassium and glycine-betaine. This allows a balance of salts inside and outside of the cell preventing water from flowing outward as would be the case if lower salt levels existed within the cells.

Acidity and Alkalinity

Yellowstone National Park has bubbling acid hotsprings that would make a witch's cauldron seem benign. They also teem with life. Once again we have been astounded that such environments harbor life.

Acidity and alkalinity are measures of the concentration of protons, the units used are pH units. The lower the number (down to zero), the higher the acidity. The higher (up to 14), the more alkaline. A neutral pH near 7 is optimal for many biological processes, although some - such as the light reactions of photosynthesis - depend on pH gradients. In nature, pH can be high, such as in soda lakes or drying ponds, or as low as 0 and below. Organisms that live at either extreme do this by maintaining the near-neutral pH of their cytoplasm (i.e.) the liquid and materials within their cells.

Low pH is the realm of acidophiles - "acid lovers". If you are looking for champion acid lovers, forget fish and cyanobacteria which have not been found below pH 4, or even plants and insects which don't survive below pH 2 to 3. The extreme acidophiles are microbes. Several algae, such as the unicellular red alga Cyanidium caldarium and the green alga Dunaliella acidophila, are exceptional acidophiles both of which can live below pH 1. Three fungi, Acontium cylatium, Cephalosporium sp., and Trichosporon cerebriae, grow near pH 0. Another species, Ferroplasma acidarmanus, has been found growing at pH 0 in acid mine drainage in Iron Mountain in California. These polyextremophiles (tolerant to multiple environmental extremes) thrive in a brew of sulfuric acid and high levels of copper, arsenic, cadmium, and zinc with only a cell membrane and no cell wall.


Octopus Spring, an alkaline (pH 8.88.3) hotspring in Yellowstone National Park, USA, is situated several miles north of Old Faithful geyser. The water flows from the source at 95°C to an outflow channel, where it cools to a low of 83°C. About every 45 minutes a pulse of water surges from the source raising the temperature as high as 88°C. In this environment the pink filamentous Thermocrinis ruber thrives.
High Temperature

Temperature is a critical parameter because it determines whether liquid water is present. If temperature is too low, enzymatic activity slows, membrane fluidity decreases. Below freezing ice crystals form that slice through cell membranes. High temperatures can irreversibly alter the structure of biomolecules such as proteins, and increase membrane fluidity. The solubility of gasses in water is correlated with temperature, creating problems at high temperature for aquatic organisms requiring oxygen or carbon dioxide.

As it happens, organisms can outwit theory. Geysers, hotsprings, fumaroles and hydrothermal vents all house organisms living at or above the boiling point of water. The most hyperthermophilic (VERY hot loving) organisms are Archaea, with Pyrolobus fumarii (of the Crenarchaeota), a nitrate-reducing chemolithotroph (an organism that derives energy from minerals), capable of growing at up to 113°C, is the current champion. As such, these hyperthermophiles are able to prevent the denaturation and chemical modification (breakdown) of DNA which normally occurs at or around a comparatively cool 70°C. The stability of nucleic acids is enhanced by the presence of salts which protect the DNA from being destroyed.

Thermophily (living in hot places) is more common than living in scalding, ultra hot locales, and includes phototrophic bacteria (i.e., cyanobacteria, and purple and green bacteria who derive energy from photosynthesis), eubacteria (i.e., Bacillus, Clostridium, Thiobacillus, Desulfotomaculum, Thermus, lactic acid bacteria, actinomycetes, spirochetes, and numerous other genera), and the Archaea (i.e., Pyrococcus, Thermococcus, Thermoplasma, Sulfolobus, and the methanogens). In contrast, the upper limit for eukaryotes is ~ 60°C, a temperature suitable for some protozoa, algae, and fungi. The maximum temperature for mosses is another 10° lower, vascular plants (house plants, trees) about 48°C, and fish 40°C.

Low Temperature

Representatives of all major forms of life inhabit temperatures just below 0°C. Think winter, think polar waters. While sperm banks and bacterial culture collections rely on the preservation of live samples in liquid nitrogen at -196°C, the lowest recorded temperature for active microbial communities and animals is substantially higher at -18°C.

Freezing of water located within a cell is almost invariably lethal. The only exception to this rule known from nature is the nematode Panagrolaimus davidi which can withstand freezing of all of its body water. In contrast, freezing of extracellular water - water outside of cells - is a survival strategy used by a small number of frogs, turtles and one snake to protect their cells during the winter. Survival of freezing must include mechanisms to survive thawing, such as the production of special proteins or "cryoprotectants" (additives that protect against the cold) called "antifreeze" proteins. The other method to survive freezing temperatures is to avoid freezing in the first place. Again "antifreeze" molecules are produced which can lower the freezing point of water 9 to 18°C. Fish in Antarctic seas manage to employ these mechanisms to their advantage.

Other changes with low temperature include changes in the structure of a cell's proteins - most notably their enzymes - so as to allow them to function at lower temperatures. The fluidity of cell membranes decreases with temperature. In response, organisms that are able to adapt to cold environments simply increase the ratio of unsaturated to saturated fatty acids thus retaining the required flexibility of membranes.

Radiation

Radiation is a hazard even on a comfortable planet like Earth. Sunlight can cause major damage unless mechanisms are in place to repair - or at least limit - the damage. Humans lacking the capacity to repair ultraviolet (UV) damage have xeroderma pigmentosa. This disease is so serious that suffers cannot leave their house during the day unless completely covered, and must even shade the windows in their homes.

Once you leave the protected surface of Earth, things can get more hostile. One of the major problems that organisms might face during interplanetary transfer (inside a rock blasted off of a planet by a large impact event for example), living on Mars, or even at high altitudes on Earth is the high levels of UV (ultraviolet) radiation.


"A "tetrad" of Deinococcus radiodurans cells.
In space there is cosmic and galactic radiation to contend with as well. The dangers of UV and ionizing radiation range from inhibition of photosynthesis up to damage to nucleic acids. Direct damage to DNA or indirect damage through the production of reactive oxygen molecules creates can alter the sequence or even break DNA strands.

Several bacteria including two Rubrobacter species and the green alga Dunaliella bardawil, can endure high levels of radiation. Deinococcus radiodurans, on the other hand is a champ and can withstand up to 20 kGy of gamma radiation up to 1,000 joules per s02. meter of UV radiation. Indeed, D. radiodurans can be exposed to levels of radiation that blow its genome into pieces only to have the organism repair its genome and be back to normal operations in a day.

This extraordinary tolerance is accomplished through a unique repair mechanism which involves reassembling damaged (fragmented) DNA. Scientists at the Department of Energy are looking to augment D. radiodurans genome such that it can be used to clean up mixed toxic and radioactive spills. So eager are biotechnologist to understand just how D. radiodurans does what it does that its genome was among the first organisms to be fully sequenced.

Gravity

Gravity is a constant force in our lives; who has not imagined what it would be like to be an astronaut escaping gravity even temporarily? The universe offers a variety of gravitational experiences, from the near absence of gravity's effects in space (more accurately referred to as microgravity) to the oppressive gravitational regimes of planets substantially larger than ours.

Gravitational effects are more pronounced as the mass of an organism increases. That being said, flight experiments have revealed that even individual cells respond to changes in gravity. Cell cultures carried aboard various spacecraft including kidney cells and white blood cells showed marked alterations in their behavior, some of which is directly due to the absence of the effects of a strong gravity field. Indeed, recent work conducted aboard Space Shuttle missions has shown that there is a genetic component (as yet understood) to kidney cell responses to microgravity exposure.


A deep ocean hydrothermal vent belching sulfide-rich hot water. The black "smoke" is created as sulfide minerals form in the mixing process between vent water and colder ocean water. These minerals settle and can accumulate to great thicknesses.
Pressure

Pressure increases with depth, be it in a water column or in rock. Hydrostatic (water) pressure increases at a rate of about one-tenth of an atmosphere per meter depth, whereas lithostatic (rock) pressure increases at about twice that rate. Pressure decreases with altitude, so that by 10 km above sea level atmospheric pressure is almost a quarter of that at sea level.

The boiling point of water increases with pressure, so water at the bottom of the ocean remains liquid at 400C. Because liquid water normally does not occur above ~100°C, increased pressure should increase the optimal temperature for microbial growth, but surprisingly pressure only extends temperature range by a few degrees suggesting that it is temperature itself that is the limiting factor.

The Marianas trench is the world's deepest sea floor at 10,898 m, yet it harbors organisms that can grow at temperature and pressure we experience everyday. It has also yielded obligately piezophilic species (i.e. organisms that are pressure loving and can only grow under high pressure) that can only grow at the immense pressures found at the ocean's greatest depths.

Other extreme conditions

A bit of creative thinking suggests other physical and chemical extremes not considered here, including unusual atmospheric compositions, redox potential, toxic or xenobiotic (manmade) compounds, and heavy metal concentration. There are even organisms such as Geobacter metallireducens that can survive immersion in high levels of organic solvents such as those found in toxic waste dumps. Others thrive inside the cooling water within nuclear reactors. While these organisms have received relatively little attention from the extremophile community, the search for life elsewhere may well rely on a better understanding of these extremes.

Extremophiles and Astrobiology

The study of extremophiles holds far more than Guinness Book of World Records-like fascination. Seemingly bizarre organisms are central to our understanding of where life may exist and where our own terrestrial life may one day travel. Did life on Earth originate in a hydrothermal vent? Will extremophiles be the pioneers that make Mars habitable for our own more parochial species?

Happily, extremophile research has lucrative side. Industrial processes and laboratory experiments may be far more efficient at extremes of temperature, salinity and pH, and so on. Natural products made in response to high levels of radiation or salt have been sold commercially. Glory too goes to those working with extremophiles. At least one Nobel Prize, that for the invention of the polymerase chain reaction (PCR), would not have been possible without an enzyme from a thermophile. As the world of molecular biology has become increasingly reliant on products from extremophiles, they will continue be the silent partner in future awards.

Current work on extremophiles in space focuses on four major environments: manned-flight vehicles, interplanetary space (because of the potential for panspermia), Mars and Europa because of the possibility of liquid water - and thus life.


This Mars Global Surveyor spacecraft photo covers an area approximately 3 kilometers (1.9 miles) wide by 6.7 km (4.1 mi) high. The image shows gullies eroded into the wall of a meteor impact crater in Noachis Terra. Channels and associated aprons of debris that are thought to have been formed by groundwater seepage, surface runoff, and debris flow.
Mars: Habitable?

Mars is, at first blush, inhospitable. Temperatures are, for the most part, frigid, exposure to ultraviolet radiation is high, and the surface is highly oxidizing, precluding the presence of organic compounds on the surface. The atmospheric pressure is very low (similar to that of Earth's uppermost atmosphere) so liquid water is unstable on the surface. Yet hydrogeological evidence from Mars Global Surveyor hints that liquid water may even flow today under the surface. Previous evidence seems to show that it once flowed much more freely on the surface in ancient times.

Could Mars harbor subsurface life, similar to the subsurface or hydrothermal communities found on Earth? If so, it would be protected from surface radiation, damaging oxidants, and have access to liquid water. Mars is rich in carbon dioxide, the raw material used by plants to produce organic carbon. Life has been found at the depths of Earth's oceans and several kilometers below the surface inside of rocks. If it did arise during a warmer, wetter period in Mars' history, perhaps it managed to migrate into warmer, more clement regions of the planet's interior before the surface became uninhabitable.

The Large Moons of Jupiter: Underground Oceans

With evidence mounting that one or more of the large moons of Jupiter (Europa, Ganymede, Callisto) have ice-covered lakes, the possibility of life on these moons becomes a subject of scientific discourse. One of these, Europa, has an ice layer too thick to allow enough light to get through to allow photosynthesis, the process that drives much of terrestrial life including those under the perennially ice-covered lakes of Antarctica. However, Chris Chyba from the SETI Institute has suggested that chemistry in the ocean's ice cover, driven by charged particles accelerated in Jupiter's magnetosphere, could produce sufficient organic and oxidant molecules for a Europan biosphere to be sustained. The Galileo spacecraft has detected a weak magnetic field on Callisto, suggesting that salt water may lie beneath an ice-covered surface. Supportive evidence exists as well for an ocean with Ganymede. Several of Saturn's moons and other outer solar system bodies may also hold the potential for having a subsurface ocean.

Naked in Space: The Ultimate Exposure

Panspermia ("seeds spread far"), the idea that life can travel through space from one hospitable location to the another, is no longer wild speculation. Space is extremely cold, subject to unfiltered solar radiation, solar wind, galactic radiation, space vacuum, and to negligible gravity. But this treacherous realm can be crossed by life. [Table II]

TABLE II. Physical conditions prevailing in the interplanetary space environment

Parameter

Interplanetary Space

Pressure (Pa)

10-14

Solar electromagnetic radiation range

all

Cosmic ionizing radiation Gy/yr)

< 0.1

Gravity

< 10-6*

Temperature (K)

4*


Over the history of the solar large impact events may have served as a steady means of transporting rocks (which arrived as meteorites) between one world or another. Whether or not any of these rocks ever actually contained viable life forms is not known. However recent studies suggest that this is possible.
We know from Mars meteorites such as the (now) famous ALH84001 sample that a natural vehicle exists for interplanetary transport. These meteorites contain organic compounds from Mars, showing that such compounds can survive the journey. Moreover, studies have shown that given a rock of sufficient size, conditions within a rock thrown off of Mars - and then later entering Earth's atmosphere - can remain cool enough such that not just organic material - but also microbes contained within - could (theoretically) survive the trip.

The criticism that life cannot endure extended periods in space is now being tested experimentally in space simulation facilities in the U.S. and Germany, and through unmanned flight experiments. NASA's Long Duration Exposure Facility and the European Space Agency's BioPan space experiments showed that microbes can survive direct exposure to the raw conditions of space. Survivors to date include spores of Bacillus subtilis and halophiles in the active (vegetative) state. Hopes for further experiments of this nature rest on both unmanned flights and the ESA Exposed Facility planned for the International Space Station.

Summary

Earth provides us with a wondrous array of life's adaptations. Indeed, by studying the extremophiles here on Earth, we may get the first clear indication of what ET could be like - or at least the range of things they might eat and breathe.

References

Norton, C. F. & Grant, W. D. Survival of halobacteria within fluid inclusions in salt crystals. J. Gen. Microbiol. 134, 1365-73 (1988).

Rothschild, L. J., Giver, L. J., White, M. R. & Mancinelli, R. L. Metabolic activity of microorganisms in gypsum-halite crusts. J. Phycol., 30:431-438 (1994).

Vreeland, R. H., Rosenzweig, W. D. & Powers, D. W. Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature 407, 897900 (2000).

Macelroy, R. D. Some comments on the evolution of extremophiles. Biosystems 6, 74-75 (1974).

Reviews:

Rothschild, L. J. & Mancinelli, R. L. Life in Extreme Environments. Nature 409: 1092-1101 (2001).

Mancinelli, R.L. & L.J. Rothschild. "Extremophiles: Who, What, Where and How". McMillan Encyclopedia of Biology, 2002. In press. Madigan, M. T. & Marrs, B. L. Extremophiles. Scientific Am. 276(4), 82-87 (1997)

Horikoshi, K. & Grant, W. D. Extremophiles. Microbial Life in Extreme Environments. (Wiley-Liss, New York 1998).

Seckbach, J., (ed.) Journey to Diverse Microbial Worlds Adaptation to Exotic Environments. (Kluwer Academic Publishers, Dordrecht 2000).


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