3

Life in Extreme Environments

A wide variety of extreme environments is known to exist on Earth, including those characterized by, for example, physical conditions such as extreme temperatures and pressures and chemical conditions such as salinity, acidity, or alkalinity. These environments are different from the preferred environment to which we human beings are adapted, yet they are inhabited by organisms that have successfully adapted to them. This chapter discusses some of these organisms, collectively known as extremophiles, and some of the environments they inhabit. Such information can provide insights into the types of terrestrial organisms that might survive and grow on Europa.

EXTREMOPHILES

Extremophiles can be categorized according to the physical characteristics of the environments in which they live. Thus, for example, the thermophiles and barophiles are found in regions characterized by high temperatures and pressures, respectively.1 The organisms most relevant to an assessment of the probability of the contamination of Europa are those capable of surviving in environments characterized by some combination of low temperatures, high pressures, and a high background radiation.

Psychrophiles and psychrotrophs are types of microorganisms that inhabit cold environments. Psychrophiles have a maximum growth temperature of 20 °C, an optimum growth temperature of 15 °C or lower, and a minimum growth temperature of 0 °C or lower,2 whereas psychrotrophs have somewhat warmer optimum and maximum growth temperatures. While both are found in many cold environments, only psychrotrophs are found where the temperature can exceed the maximum growth temperature of the psychrophiles in question. In many polar environments, for example, radiant energy can increase the temperature above the maximum growth temperature for psychrophiles, and as a result they expire. This is probably the main reason no psychrophiles are found in the terrestrial portions of Antarctica. Their abnormal susceptibility to warm temperatures means that they are unlikely to be present in a spacecraft-assembly environment and are therefore unlikely to contaminate a spacecraft.

Psychrotrophs, on the other hand, can be found in any environment, and most of the early research on these organisms was carried on by food microbiologists. Various species of psychrotrophs are in well-known genera such as Pseudomonas, Flavobacterium, Achromobacter, Alcaligenes, Bacillus, Arthrobacter, and Vibrio. Microbial ecologists have found them in most cold environments, even in the harsh desert environments of Antarctica.3 These organisms can also be found in permafrost as well as in the deeper layers of ice cores, indicating that they have the ability to survive for extremely long periods of time. Laboratory studies indicate that not all species can survive the freezing and thawing process, and many species are killed when frozen, especially if they are in the exponential growth phase.

The best estimate for the minimum temperature of microbial growth is -10 to -12 °C (although there are a few reports of growth at lower temperatures), and this low temperature has been recorded for only a few bacteria. This minimum temperature for growth appears to be determined by the fluidity of cell membranes and the availability of liquid water. If an organism cannot desaturate its membrane lipids, the cellular transport of substrates ceases. The freezing property of the liquid within and immediately adjacent to the cell also comes into play. Either factor can prevent the cell from growing. It is extremely doubtful that any organism can grow at 100 K, but survival remains a possibility at any depth in Europa’s ice.

Psychrotrophs may survive at the surface temperatures of Europa, as indicated by current techniques that employ freezing for preserving microbial cells. Europa’s geologic conditions may not change significantly for a long period of time and so the microbes might have to stay in this survival state for millions of years. Surviving microbes might have extreme difficulty initiating growth owing to the absence of organic matter for heterotrophic growth and their inability to metabolize at 100 K. The absence of an organic matter energy source does not, however, rule out the possibility of psychrotrophic chemoautotrophic growth if the organism can reach subsurface liquid water.



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Preventing the Forward Contamination of Europa 3 Life in Extreme Environments A wide variety of extreme environments is known to exist on Earth, including those characterized by, for example, physical conditions such as extreme temperatures and pressures and chemical conditions such as salinity, acidity, or alkalinity. These environments are different from the preferred environment to which we human beings are adapted, yet they are inhabited by organisms that have successfully adapted to them. This chapter discusses some of these organisms, collectively known as extremophiles, and some of the environments they inhabit. Such information can provide insights into the types of terrestrial organisms that might survive and grow on Europa. EXTREMOPHILES Extremophiles can be categorized according to the physical characteristics of the environments in which they live. Thus, for example, the thermophiles and barophiles are found in regions characterized by high temperatures and pressures, respectively.1 The organisms most relevant to an assessment of the probability of the contamination of Europa are those capable of surviving in environments characterized by some combination of low temperatures, high pressures, and a high background radiation. Psychrophiles and psychrotrophs are types of microorganisms that inhabit cold environments. Psychrophiles have a maximum growth temperature of 20 °C, an optimum growth temperature of 15 °C or lower, and a minimum growth temperature of 0 °C or lower,2 whereas psychrotrophs have somewhat warmer optimum and maximum growth temperatures. While both are found in many cold environments, only psychrotrophs are found where the temperature can exceed the maximum growth temperature of the psychrophiles in question. In many polar environments, for example, radiant energy can increase the temperature above the maximum growth temperature for psychrophiles, and as a result they expire. This is probably the main reason no psychrophiles are found in the terrestrial portions of Antarctica. Their abnormal susceptibility to warm temperatures means that they are unlikely to be present in a spacecraft-assembly environment and are therefore unlikely to contaminate a spacecraft. Psychrotrophs, on the other hand, can be found in any environment, and most of the early research on these organisms was carried on by food microbiologists. Various species of psychrotrophs are in well-known genera such as Pseudomonas, Flavobacterium, Achromobacter, Alcaligenes, Bacillus, Arthrobacter, and Vibrio. Microbial ecologists have found them in most cold environments, even in the harsh desert environments of Antarctica.3 These organisms can also be found in permafrost as well as in the deeper layers of ice cores, indicating that they have the ability to survive for extremely long periods of time. Laboratory studies indicate that not all species can survive the freezing and thawing process, and many species are killed when frozen, especially if they are in the exponential growth phase. The best estimate for the minimum temperature of microbial growth is -10 to -12 °C (although there are a few reports of growth at lower temperatures), and this low temperature has been recorded for only a few bacteria. This minimum temperature for growth appears to be determined by the fluidity of cell membranes and the availability of liquid water. If an organism cannot desaturate its membrane lipids, the cellular transport of substrates ceases. The freezing property of the liquid within and immediately adjacent to the cell also comes into play. Either factor can prevent the cell from growing. It is extremely doubtful that any organism can grow at 100 K, but survival remains a possibility at any depth in Europa’s ice. Psychrotrophs may survive at the surface temperatures of Europa, as indicated by current techniques that employ freezing for preserving microbial cells. Europa’s geologic conditions may not change significantly for a long period of time and so the microbes might have to stay in this survival state for millions of years. Surviving microbes might have extreme difficulty initiating growth owing to the absence of organic matter for heterotrophic growth and their inability to metabolize at 100 K. The absence of an organic matter energy source does not, however, rule out the possibility of psychrotrophic chemoautotrophic growth if the organism can reach subsurface liquid water.

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Preventing the Forward Contamination of Europa Barophiles are microorganisms that thrive under conditions of high hydrostatic pressure, and all known examples inhabit marine environments. Europa’s ice shell may be 10 to 170 km thick, and thus the pressure in the upper layers of a hypothetical europan ocean would have to be 13 to 210 MPa (130 to 2,100 bars), assuming that the ice has the same density as water. Studies indicate that most organisms cannot grow when the pressure exceeds 60 MPa, and many are indeed killed at that pressure. Known terrestrial organisms could withstand the pressure near the top of Europa’s putative ocean, especially if the ice shell is relatively thin. A combination of high pressure and low temperature would, however, decrease the molecular volume of a microbe’s macromolecules and would probably bring about its death. For example, Bacillus subtilis, one of the indicator organisms currently used to determine the bioload on a spacecraft (see Chapter 5), can survive pressures of 30 MPa provided that the temperature is greater than 20 °C. Radiation-resistant organisms are of particular relevance to any discussion of the forward contamination of Europa. The bacterium Deinococcus radiodurans, for example, can grow continuously, without mutation or any effect on its growth rate, in the presence of 6,000 rad/hr (a dose rate found 1 mm beneath Europa’s surface ice).4 This organism can also survive acute exposures to ionizing radiation of 3 Mrad (at -70 °C) without lethality—a dose that induces about 130 double-strand breaks (DSBs) per chromosome. Furthermore, viable cells are readily recovered from cultures even after exposure to 8 Mrad (at -70 °C).5 This ability is extraordinary since most cells cannot survive irradiation at more than 500 to 100,000 rad6or 1 to 3 DSBs per haploid chromosome.7Recent advances have led to insights into this bacterium’s exceedingly efficient DNA repair capabilities,8,9which have been shown to be partly responsible for its resistance to radiation.10,11 Because there are no known radioactive environments that can explain the evolution of D. radiodurans’s resistance to radiation, there is general agreement that this organism ’s resistance to radiation is a secondary characteristic developed in response to some other environmental stress. The consensus view is that the mechanisms that evolved to permit survival in very dry environments also confer resistance to radiation.12 It is possible that other desiccation-resistant microorganisms, not yet described as radiation-resistant, could pose a threat to the europan biosphere. Such organisms can only pose a threat if they can survive a multi-year journey to Europa. Despite the discrediting of the oft-repeated claim that live bacteria were recovered from Surveyor 3’s camera after surviving on the Moon’s surface from April 20, 1967, to November 20, 1969, experiments conducted aboard a variety of spacecraft including the European Retrievable Carrier and the Long Duration Exposure Facility indicate that a variety of common terrestrial bacteria are able to withstand the space environment for periods as long as 6 years.13,14Since the radiation-resistance characteristics of many common organisms (and most extremophiles) are unknown, it is conceivable that many bacteria classified as desiccation-and/or radiation-resistant will survive in extraterrestrial environments. On Europa, life-sustaining, near-surface environments may exist within or under regions of water ice, since ice will provide microbes with some degree of radiation protection. In addition to requiring water in the liquid state, genetic repair would certainly also be dependent on the presence of a source of carbon and energy. There is currently little or no evidence for any organic matter on Europa’s surface due to the lack of observable spectral features of CH bonds in Galileo ’s infrared spectra of Europa. Nevertheless, the presence of carbon in material recycled from the interior via geologic processes or in cometary and meteoritic debris cannot be discounted.15 EXTREME ENVIRONMENTS The ability (or inability) of terrestrial organisms to adapt to, and survive and multiply in, extreme terrestrial environments reveals much about the resilience of life in stressful circumstances. Given that these organisms have had millions of years to come to terms with their particular physical and chemical environments, their ability to cope provides some insight into the problems facing terrestrial organisms suddenly introduced into extraterrestrial environments. Earth’s polar regions present two particularly telling examples, the cryptoendolithic environments found in the polar deserts and permafrost. Antarctic cryptoendolithic environments exist where communities of microorganisms have colonized the surface layers of porous rocks to depths of a few millimeters. Photosynthetic members of the community utilize sunlight that penetrates the translucent rock crust. The ambient air in the Antarctic desert is rarely above 0 °C, but the near-surface regions of rocks exposed to the Sun are warmed by solar radiation. The cryptoendolithic colonies obtain water from snow, which melts when it falls on warm and dry rock surfaces.

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Preventing the Forward Contamination of Europa The cryptoendolithic environments are good examples of absolute extreme environments, i.e., regions where the physical conditions are beyond adaptability. The organisms colonizing the rocks are not adapted to their environment; they survive by tolerating it. While all metabolic activity occurs at ~±10 °C, the optimum temperatures for organisms, as measured in the laboratory, range from 15 to 25 °C, temperatures rarely reached in the Antarctic. Thus microorganisms in Antarctic rocks live near the lower limits of their physiological potential, and they have no reserves to compensate for changes in the environment, should conditions deteriorate. As a consequence, even a minor change in climate can result in local extinctions. In fact, close to 80 percent of the cryptoendolithic communities in Antarctica are dead or fossilized.16 Permafrost microorganisms have been studied most extensively in Siberia 17and have recently been found in Antarctica.18Permafrost microorganisms originate in the soil where they have been immobilized by freezing, while new soil continues to be formed on the surface. In Siberia, the oldest permafrost is 3.5 million to 5 million years old. Recent drilling in Antarctica revealed permafrost some 8 million years old. Permafrost temperatures are extremely stable, around -10 °C in Siberia and down to about -30 °C in Antarctica. The number of viable bacteria (up to 10 million colony-forming units per gram of dry weight) and the abundance of species found in permafrost decrease with increasing depth (i.e., with increasing age). The viable microbial community in permafrost—mostly psychrotrophs and only very few psychrophiles—is dominated by prokaryotes (organisms whose cells lack a nucleus). Eukaryotic algae (i.e., algae whose cells contain a nucleus) do not survive beyond 5,000 to 7,000 years, but viable yeasts are found in 3 million-year-old permafrost. The composition of bacterial communities found in permafrost mirrors that of the soil from which they originate. Most bacteria isolated from permafrost are aerobes; only a few are anaerobes, mostly methanogens. Permafrost at -10 °C and below is frozen solid. Yet a thin film of unfrozen water envelopes both the inorganic soil particles and microorganisms. The thickness of this unfrozen water film is temperature-dependent and is reduced to about 0.5 nm at -5 °C and below. In permafrost, microbial growth is in a stationary phase and cell division probably does not occur. This, together with the fact that the number of species decreases with age, suggests that in permafrost a slow selection process takes place, and bacteria that are not able to tolerate the physical conditions of their environment eventually become extinct. In permafrost there is no adaptation, only selection. REFERENCES 1 R.A. Herbert, “A Perspective on the Biotechnological Potential of Extremophiles, ” Trends in Biotechnology 10: 395 1992. 2 R.Y. Morita, “Psychrophilic Bacteria,” Bacteriology Review 30: 144, 1975. 3 E.I. Friedmann, Antarctic Microbiology, Wiley-Liss Inc., New York, N.Y., 1993. 4 C.Lange, L. Wackett, K. Minton, and M.J. Daly, “Construction and Characterization of Recombinant Deinococcus radiodurans for Organopollutant Degradation in Radioactive Mixed Waste Environments, ” Nature Biotechnology 16: 929, 1998. 5 M.J. Daly, personal communication. 6 K.W. Minton and M.J. Daly, “A Model for Repair of Radiation Induced DNA Double-Strand Breaks in the Extreme Radiophile Deinococcus radiodurans,” Bio Essays 17: 457, 1995. 7 F. Krasin and F. Hutchinson, “Repair of DNA Double-Strand Breaks in Escherichia coli, Which Requires recA Function and the Presence of a Duplicate Genome,”Journal of Molecular Biology 116: 81, 1977. 8 M.J. Daly et al., “In Vivo Damage and RecA-Dependent Repair of Plasmid and Chromosomal DNA in the Radioresistant Bacterium Deinococcus radiodurans,” Journal of Bacteriology176: 3508, 1994.

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Preventing the Forward Contamination of Europa 9 V. Mattimore and J.R. Battista, “Radioresistance of Deinococcus radiodurans: Functions Necessary to Survive Ionizing Radiation Are Also Necessary to Survive Prolonged Desiccation,” Journal of Bacteriology 177: 5232, 1996. 10 M.J. Daly et al., “In Vivo Damage and recA-Dependent Repair of Plasmid and Chromosomal DNA in the Radioresistant Bacterium Deinococcus radiodurans,” Journal of Bacteriology 176: 3508, 1994. 11 M.J. Daly and K.W. Minton, “An Alternative Pathway for Recombination of Chromosomal Fragments Precedes recA-Dependent Recombination in the Radioresistant Bacterium Deinococcus radiodurans, ” Journal of Bacteriology,178: 4461, 1996. 12 V. Mattimore and J.R. Battista, “Radioresistance of Deinococcus radiodurans: Functions Necessary to Survive Ionizing Radiation Are Also Necessary to Survive Prolonged Desiccation,” Journal of Bacteriology 177: 5232, 1996. 13 R.L. Mancinelli, M.R. White, and L.J. Rothschild, “Biopan-Survival I: Exposure of the Osmophiles Synechococcus Sp. (Nageli) and Haloarcula Sp. to the Space Environment,” Advances in Space Research 22: 327, 1998. 14 G. Horneck, “Exobiological Experiments in Earth Orbit,” Advances in Space Research 22: 317, 1998. 15 S.J. Mojzsis and G. Arrhenius, “Early Mars and Early Earth: Paleoenvironments for the Emergence of Life,”Proceedings of the International Society for Optical Engineering 3111: 162 1997. 16 E.I. Friedmann, A.Y. Druk, and C. McKay, “Limits of Life and Microbial Extinction in the Antarctic Desert,”Antarctic Journal of the United States 29(5): 176, 1994. 17 T. Shi et al., “Characterization of Viable Bacteria from Siberian Permafrost by 16S rDNA Sequencing,” Microbial Ecology 33: 169, 1997. 18 G.S. Wilson et al., “Coring for Microbial Records of Antarctic Climate,” Antarctic Journal of the United States, Review 1996 31: 83, 1998.