The word "extreme" comes from the Latin word "extremus," the superlative of "exter" (= on the outside) (Rothschild and Mancinelli, 2001). Whereas there is no general agreement on how to define an extreme environment, the term is commonly used for any setting that exhibits life conditions detrimental or fatal to higher organisms with respect to its physicochemical properties. Thus, extreme environments differ in one or more aspects from those which humans consider as "normal," moderate conditions with circumneutral pH, temperatures between 20°C and 35°C, pressures around 0.1 MPA (1 atm), and adequate concentrations of nutrient and saline. It should be considered, however, that such definition represents an anthropocentric view and that what is extreme and what is normal from a microbial perspective remains questionable.
If not completely uninhabitable to life, extreme environments typically harbor specially adapted organisms, the so-called extremophiles. Most extremophiles are unicellular organisms, that is, protists, bacteria, and archaea. As a rule, extreme environments show a low diversity of multicellular organisms and only few animals are able to withstand the harsh conditions of particular extreme environments. Terms describing extremophiles usually combine an environment-specific prefix with the suffix "-phile" (Greek word for "-loving"). Replacing the suffix "-phile" by "-tolerant" implies that an organism tolerates rather than requires the respective conditions, and actually has its optimum at more moderate conditions. Prefixes may be combined for organisms that thrive in more than one extreme (e.g., "thermoacidophiles"). Such organisms are termed polyextremophiles.
Extreme environments can be categorized into several classes.
Environments below pH 5, including, for example, sulfuric pools, geysers, and areas polluted by acid mine drainage are called acidic environments. Organisms dependent on acidic conditions below pH 5 (pH 7 = neutral) are called acidophiles. Examples are the bacterial genus Acidithiobacillus (used in biomining, see entry), Ferroplasma acidophilum, a sulfuric-acid producing archaeon involved in acid mine drainage (see entry Acid Rock Drainage ), the red alga Cyanidium caldarium (the most heat and acid tolerant alga known), the green alga Dunaliella acidophila, the fungus Trichosporon cerebriae, and the archaeum Picrophilus (Rothschild and Mancinelli, 2001). The major challenge for these organisms is to maintain their internal cellular pH at a constant, circumneutral level, that is, around pH 7. Individual strategies encompass, inter alia, (i) reinforcement of the cell membrane, (ii) secretion of extracellular polymeric substances (EPS) (see entry " Extracellular Polymeric Substances (EPS) ") to limit proton diffusion into the cell, (iii) secretion of buffer molecules capable of sequestering protons, including, for example, basic amino acids (lysine, histidine and arginine), and (iv) the ability to actively pump protons out of the cell (for reviews, see Baker-Austin and Dopson, 2007; Rothschild and Mancinelli, 2001).
Extreme Environments. Figure 1 Examples and features of extreme environments. (Images courtesy of J. Reitner and G. Arp) (a) A volcanic hot spring on Iceland, providing an environment for thermophilic bacteria and archaea. The spring bottom shows a temperature zonation of brown and black microbial mats. (b) Mono Lake, California, is an excellent example for both a hypersaline and an alkaline environment. Being a terminal lake, Mono Lake has no outlet to the ocean, and dissolved salts in the runoff have increased the water's alkalinity (pH ∼10) and salt concentration (70‰). (c) Underwater view of the ∼2 m deep hypersaline Lake 21 on Christmas Island (Republic of Kiribati). Kiritimati is a raised atoll, with a rather arid climate. Periodically flooding with sea water and subsequent evaporation cause the salinity of numerous inland lakes to increase to values about 120‰, four times that of sea water. The lake bottom is covered with microbial mats dominated by Cyanobacteria at the surface. (d) A calcifying microbial mat from the same setting as in (c), showing a complex layering of differently pigmented microbes. In the deeper parts of the mat, carbonate precipitation proceeds under anaerobic conditions, ultimately producing massive microbialites. (e) The Bonneville Salt Flats in northwestern Utah, USA, are a remnant of the ancient glacial Lake Bonneville. Up to 1.8 m, thick salt crusts provide an extremely hypertonic environment for halo- and xerophilic microorganisms. (f) Lake Clifton, 120 km south of Perth (Western Australia), provides a fragile ecosystem where the growth of a large thrombolite reef (see "Microbialites") is sustained by calcium carbonate rich aquifers water and strong seasonal trends in salinity (salinity 30-80 ‰). Notably, these modern thrombolitic microbialites coexist with a diverse invertebrate fauna.
Environments with salt concentrations greater than that of seawater (35‰; Figure 1, see also Chapters " Saline Lakes ", " Deep Biosphere of Salt Deposits ") are called hypersaline environments. Organisms dependent on salt concentrations greater than 35‰ (sea water) are called halophiles. Halophiles are known from the Archaea, Bacteria, and Eukarya (Grant et al., 1998; Gunde-Cimerron et al., 2005). Eukaryotes are represented, for instance by the green alga Dunaliella, and even animals occur in hypersaline environments, although in low species diversity (e.g., the brine shrimp Artemia, and the salt fly Ephydra). In the bacterial domain, halophiles represent many different taxonomic groups, whereas those in the archaeal domain fell into a single order (Halobacteriales) and family (Halobacteriacae; DasSarma and DasSarma, 2008). The most significant challenge for halophiles is to prevent the loss of water from the cell into the saline environment, and the accumulation of excess salt concentrations within the cell. The latter may give rise to the collapse of proteins and macromolecules, because the electric charges of the salt ions disturb the electrostatic interactions within biomacromolecules. Halophiles basically use two strategies to tackle these challenges. (i) Halophilic bacteria and algae accumulate organic compatible solutes, polar, highly soluble molecules uncharged at physiological pH, such as amino acids and their derivatives to counterbalance the osmotic pressure of the surrounding medium (Galinski, 1993; Oren, 1999). (ii) Halophilic archaea, thriving at NaCl concentrations higher than 1.5 M, use the so-called "salt-in strategy." These most halophilic organisms concentrate K+ ions within the cell in order to balance osmotic pressure. Their proteins are particularly rich in acidic amino acids, thus enhancing resistance against structural collapse. For more information, see entry " Halobacteria - Halophiles ." Several reports provided evidence that viable extremely halophilic microorganisms were enclosed in ancient salt sediments. Please refer to " Deep Biosphere of Salt Deposits " for details.
Extremely hot environments
Environments periodically or consistently above 40°C are called extremely hot environments (Stetter, 1998). Depending on the temperature, these settings harbor thermophiles (growth optimum 45-80°C, Martinko and Madigan, 2006) or hyperthermophiles (growth optimum above 80°C). (Organisms dependent on moderate temperatures between 10°C and 50°C (optimum 30-40°C) are called mesophiles.) Whereas thermophiles have a fairly broad ecological amplitude, including, for example, hot waters, sun-heated soils, and waste dumps, hyperthermophiles mostly occur at water-containing, geothermally heated terrestrial and marine springs and sediments (Figure 1a). As a rule, prokaryotes are able to grow at higher temperatures than eukaryotes (limit ∼65°C). Accordingly, hyperthermophilic life is mainly represented by deeply branching bacteria, (e.g., Aquifex, Thermotoga) and archaea (e.g., Sulfolobus, Methanothermus; Stetter, 1998). The highest commonly accepted temperature for life has been reported for the hyperthermopiezophilic archaeon Methanopyrus kandleri (122°C; Takai et al., 2008). The challenge for organisms living in hot environments lies in avoiding thermal degradation of cellular biomacromolecules, which may, for example, result in unfolding of proteins. Individual strategies encompass stabilization of proteins by introducing additional disulfide bridges, ionic interactions, hydrogen bonds, and hydrophobic interactions. Another alternative is to introduce the proline residue at particular sites into proteins (the proline rule; Imanaka, 2008). Because many scientists believe that prebiotic molecules and the first living organisms originated in hot environments, hyperthermophiles may provide insight into the early stages of life on Earth. Please refer to " Hydrothermal Environments, Terrestrial ," " Hydrothermal Environments, Marine ," " Hot Springs and Geysers ," and " Origin of Life " for further reading.
Environments under extreme hydrostatic or petrostatic (rock) pressure are high-pressure environments. Organisms thriving in these settings are called piezophiles (formerly barophiles). Broadly spoken, piezophiles organisms dependent on pressures greater than atmospheric pressure (0.1 MPa, Yayanos, 1998), although organisms living, for example, in shallow coastal waters are commonly neither considered as piezophiles nor as extremophiles. Based on their optimal growth pressure, piezophiles have further been classified as piezotolerant (0.1-10 MPa; 10MPa ≈ 1,000 m water depth), piezophilic (10-50 MPa), and hyperpiezophilic (>50 MPa) bacteria and archeaea (Fang and Bazylinski, 2008). Whereas, as a rule, the relative growth rate of these organisms decreases with pressure, the upper pressure limit of life has not yet been determined (Yayanos, 1998; Schrenk et al., 2010). High pressures affect biological systems by making the structures (e.g., membranes) more compact, as opposed to the effects of high temperature. Pressurization hinders any process resulting in a positive volume change, and vice versa. For example, if a reaction is accompanied by a volume decrease of 300 mL mol−1, it is enhanced more than 200,000-fold by applying a pressure of 100 MPa (≈10,000 m water depth; Abe et al., 1999). Likewise, hydrostatic pressure has been shown to exert a considerable influence on many protein-protein interactions, the efficacy of enzymatic catalysis, replication, and translation. Piezophiles have therefore evolved specific adaptations, for example, in terms of membrane lipid composition and cell division. Pressure has also a significant effect on microbial-mediated redox reactions, and metabolic versatility appears to be a specific adaptation to deep environments (Fang and Bazylinski, 2008; Lauro and Bartlett, 2008). For detailed reading, please refer to entry "Piezophilic Bacteria."
Extremely cold environments
Environments with temperatures below 5°C for prolonged periods of time, such as cold polar regions, glaciers, sea-ice, deep-sea sediments, and permafrost soils are considered extremely cold environments. Organisms capable of growth and reproduction in these settings are called psychrophiles (cryophiles). They depend on low temperatures (< 0°C to 20°C) and have a growth optimum below 15°C (Morita, 1975). The lowest temperature limit for life seems to be around −20°C and has been reported for bacteria living in permafrost soil and in sea-ice (D'Amico et al., 2006). Psychrophiles are found in all three domains of life. Eukaryotes such as algae (e.g., sea-ice diatoms, the "snow alga" Chlamydomonas nivalis), protozoans, fungi, and even small metazoans frequently occur, but psychrophiles are most abundant among diverse lineages within the bacteria (e.g., Pseudomonas spp., Vibrio spp., several cyanobacterial genera) and, less often cited, archaea (e.g., Methanogenium and Methanococcus) (Garrison, 1991; D'Amico et al., 2006). Main cold-induced challenges posed to psychrophiles within their habitats encompass (i) reduced enzyme activity, (ii) decreased membrane fluidity, (iii) altered transport of nutrients and waste products, (iv) decreased rates of transcription, translation, and cell division, (v) protein cold-denaturation and inappropriate protein folding, (viii) intracellular ice formation, and (ix) low water availability (see D'Amico et al., 2006, for a review). Psychrophilic organisms have successfully evolved strategies to overcome these negative effects of low temperatures. Such strategies involve modifications of the cell membrane composition toward a higher content of unsaturated, branched, or short-chain fatty acids, and large polar head groups (Chintalapati et al., 2004). Psychrophiles also synthesize specific antifreeze proteins, trehalose, and extracellular polymeric substances (EPS), which play an important role as cryoprotectants to keep the intercellular space liquid and protect the DNA at temperatures below water's freezing point (see D'Amico et al., 2006, for a review). For further reading, please refer to " Permafrost Microbiology ."
Extremely dry environments
Environments without free water are considered extremely dry environments and they include hot and cold deserts, and some terrestrial endolithic habitats (see also Chapter " Endoliths "). Organisms dependent on very dry environments are termed xerophiles, whereas those tolerating only temporary desiccation are referred to as "xerotolerant." Most organisms thriving in very dry environments are actually xerotolerants, which rely on at least periodically available free water. A strategy to cope with prolonged periods of dryness is to enter the state of anhydrobiosis, which is characterized by little intracellular water and no metabolic activity. Organisms that can become anhydrobiotic are found among bacteria, yeast, fungi, plants, and even animals such as nematodes and the brine shrimp Artemia salina (Rothschild and Mancinelli, 2001). The terms "xerophile" and "xerotolerant" are often used to include organisms thriving under conditions of low water activity aw < 0.80). The aw is a measure of the amount of water within a medium that an organism can use to support growth. It represents the ratio of the water vapor pressure of the substrate to that of pure water under the same conditions and is expressed as a fraction (pure water, aw = 1; saturated NaCl, aw = 0.75). The lowest aw value recorded for growth to date was reported for the spoilage mould Xeromyces bisporus (aw = 0.61; see Grant, 2004 for a review). According to this definition, the most xerophilic organisms known, thrive in foods preserved by some form of dehydration or enhanced sugar levels, and in hypersaline environments where water availability is limited by a high concentration of salts (Grant, 2004). Whereas the former are dominated by xerophilic filamentous fungi and yeasts, high-salt environments are almost exclusively populated by prokaryotes. For the strategies employed by these organisms to cope with the osmotic stress exerted by these environments see above, and entry " Halobacteria - Halophiles ."
Environments exposed to high doses of ionizing radiation are high-radiation environments. Ionizing radiation is radiation with sufficient energy to ionize molecules, most commonly ultraviolet (UV) radiation and natural radioactivity. When such radiation passes through (living) matter, ions and free radicals are produced that react rapidly and modify molecules (Cox and Battista, 2005). Ionizing radiation is therefore potentially detrimental for life, mainly due to DNA damage resulting from the generation of reactive oxygen species and the hydrolytic cleavage of water. Organisms that are capable of withstanding high doses of ionizing radiation are called radioresistant. There is no clear pattern of evolution among ionizing-radiation-resistant species, and they occur scattered over the three domains of life. Well-studied microbial examples are the archaeon Thermococcus gammatolerans (Jolivet et al., 2003) and the bacterium Deinococcus radiodurans (Cox and Battista, 2005). Strategies to adapt to high doses of ionizing radiation involve (i) increasing the numbers of genome copies, (ii) tight spatial arrangement of nucleoids, (iii) accumulation of efficient radical scavengers, (iv) delaying DNA replication until damage repair has been completed, and (v) improved enzymatic genome-repair process. For further reading, please refer to entry "Radioactivity."
"Extreme environment" refers to any setting that exhibits life conditions detrimental or fatal to higher organisms with respect to its physicochemical properties, in particular pH, temperature, pressure, saline concentrations, and radiation. Major classes of extreme environments encompass acidic (pH < 5), alkaline (pH > 9), hypersaline (salinity > 35‰), pressurized (> 0.1 MPa), hot (> 40°C), cold (<5°C), dry (aw < 0.80), and high-radiation environments. These environments typically harbor specially adapted organisms, the so-called extremophiles. These can be classified into acidophiles, alkaliphiles, (hyper-)thermophiles, psychrophiles, xerophiles, and radioresistant organisms.
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