Open any biology textbook from 1976 to its first chapter and you’ll likely find the same assumptions on the basic needs of life: life requires oxygen, sunlight, water, moderate temperatures, and moderate pressures to survive. These texts might note some more extreme forms of life like bacteria in hot springs, but would always note that they still depend on ambient ecosystems. At the time, very few scientists considered novel energy sources or environments, and no real conjecture about unique metabolisms existed.
When hydrothermal vents were discovered off of the Galapagos Islands in 1977, scientists worldwide reconsidered their basic assumptions about life’s limits. Here, life thrived without sunlight and photosynthesis at extreme temperatures and pressures. Subsequent exploration of these vents has shown that these forms of life are not only ubiquitous but also may be the most ancient and conserved species (1). Further studies have continuously upped the ante: how extreme is too extreme? What sorts of conditions are tolerable? This trend has led scientists to think as broadly as possible about limits to life and to imagine metabolisms that work at the most extreme chemical and physical boundaries. Since 1977, extremophilic studies have compelled new understandings of the nature and origin of life on Earth and within the universe. Although ordinary microbes activate specific survival proteins under environmental stresses, what distinguishes extremophiles are their “extreme” optimal growth conditions, and the specific proteins, membranes, or mechanisms that have evolved for their niche. Extremophiles are typically grouped by the specific niche they occupy: halophiles for salinity, alkaliphiles and acidophiles for high and low pH, thermophiles for high temperature, and barophiles for pressure. For example, the methanogen methanothermobacter wolfei (like most methan gens) needs to be incubated at 60 °C to be grown in the laboratory as a result of its compact protein structures. Like any other organism, without the proper environment, these methanogens die.
Life has evolved to inhabit every environment that has been discovered on Earth. Some particularly extraordinary environments include salt flats, Arctic lakes and ices, and the interior of rocks. Some organisms have even been discovered thriving in man-made environments such as smoldering coal refuse and geothermal power plants (2).
Investigating the life found in these unique places reveals insights about microbial diversity and metabolism. For example, halophiles increase internal osmolarity, the prevention of water escape by osmosis, by diluting the cytoplasm with organic solutes, by selectively taking up potassium ions, or by having charged amino acids on cell surfaces (3). In low pH environments, acidophiles maintain a multi-levelled pH gradient across the cellular membrane, which maintains a roughly neutral pH in the cytoplasm (2). And radio-resistant microbes that resist mutation in intense UV environments have evolved extraordinarily efficient DNA repair mechanisms (4).
Of particular interest are barophilic (pressure-loving) organisms. These microbes evolved mechanisms for enduring high hydrostatic pressure and indeed can survive pressures up to thousands of atmospheres (5). Barophiles have wide range pressure-activated gene sequences, which can code for more compact protein structures, increased membrane strength (6), and increased resistance in enzymes and metabolites (7, 8). What is most remarkable about these organisms, however, is that their pressure threshold increases with increasing temperature. These two thermodynamic variables counteract each other, so that microbes can survive and might even metabolize at pressures and temperatures found in planetary interiors. Some scientists are beginning to investigate whether the true pressure/temperature limit to life is purely thermodynamic: at approximately 10,000 atmospheres and greater than 120°C, water reverts to a solid ice phase. This crystallization would inhibit mobility and nutrient mobilization, and might therefore be the true thermodynamic limit (9). These barophiles—still barely explored—demonstrate that life might exist at the very limits of thermodynamics. We can imagine, therefore, that life outside of the Earth system can endure equally—if not more so–extraordinary conditions.
In addition to discovering increasingly extreme limits to life, scientists have also discovered an increasingly wide range of energy sources. Only within the last few decades have scientists looked beyond the most typical sunlight-dependent, photosynthesizing, glucose-burning forms of life. This exploration has not only yielded new forms of microbes, but has also unearthed countless new forms of microbial energy acquisition and utilization (10).
Initially, the discovery of novel electron donors and acceptors shook the microbiological community, yet it is now widely known that different strains of microbes can use ferric iron, manganese oxide, uranium oxide, sulfate, nitrate, iron sulfides, and virtually any oxidized chemical compound as terminal electron acceptors. The range of electron donors is equally as extensive: any reduced species—methane, acetate, formate, ferrous iron, ammonium—may act as a reductant in microbial metabolism. Most strains are best adapted to utilize one electron donor and one acceptor, but it has been found that most microbes can identify and utilize a wide range of molecules in metabolism. The Shewanella group of bacteria, for example, uses oxidized forms of iron, cobalt, manganese, chromium, uranium, and technetium as electron acceptors (11).
Moreover, some microbes can even reverse typical processes. While most life on Earth typically uses the citric acid cycle to reduce oxygen and generate energy, some anaerobic chemolithoautotrophs reverse this cycle to produce energy and generate reduced species such as methane or acetate. Other recently discovered metabolisms utilized by chemolithoautotrophs include the reductive acetyl co-A cycle, the 3-hydroxypropionate/malyl-coA cycle, and the 4-hydroxybutyrate cycle. These microbes and their various forms of energy acquisition have widely expanded the microbiological community’s conception of metabolism and the diversity of microbial life.
Additionally, it has been demonstrated that practically any energy gradient can be harnessed by life. Redox gradients have been thoroughly studied, and indeed the unique oxidation/reduction pathways discussed above are often utilized to take advantage of the various metal species found at redox gradients. Thermal gradients have also been explored. In order to harness thermal energy, microbes might use the primordial protein pF1, which functioned on a thermal variation of the protein ATP synthase (12). This idea could be applied widely to planetary bodies that lack the proper chemical or photo energy sources.
The final unique energy source so far proposed by scientists is radioactive decay. According to the theory, hydrogen would be liberated from the rock via decay of uranium, thorium, and potassium, and then could be used as a reductant in lithoautotrophic metabolism. The scientists who discovered deep-Earth bacteria (~3 km below the surface) argue that this was most likely their energy source (13, 14). Other scientists have highlighted the importance of Fischer-Tropsch organic synthesis reactions in planetary interiors. The combination of organic material from these reactions and energy from radioactive decay may provide means by which life could originate in planetary interiors (15). Since each terrestrial planet we know of is full of radioactive elements Rb, Sm, Al, U, Pb, K, etc, and since carbon is ubiquitous as well, studying these processes may yield insight into the possibility for life inside terrestrial planets.
Studies of unique energy sources and the metabolisms that might utilize them have vastly expanded the range of worlds possibly inhabited in the universe. Even though life on Earth continues to surprise and impress scientists, observed life forms no longer restrict them from creatively imagining new metabolisms. Each environment with liquid water, carbon, and a physical or chemical gradient is now under serious consideration for life. This has led NASA to send probes not only to Venus and to Mars, but to Saturn’s and Jupiter’s moons, which were originally long shots in the search for life. Now, the water-saturated Europa, and methane/hydrocarbon-saturated Titan are front runners in the considerations for life in this solar system (16).
Furthermore, if radioactive decay or even simple oxidation or reduction of material can provide the energy required for life in the interior of planets, then any terrestrial planet may play host to life. If a given planet contains water, carbon dioxide, and transition metals, it contains all the reactants and catalysts required for complex organic synthesis. These requirements are flexible and present almost everywhere in the universe.
Therefore, microbiology is rapidly expanding to include both geologic and astronomical studies. Other worlds and imaginative life forms are being explored, and this is due to decades of collaboration by scientists in fields as far apart as genetics, genomics, proteomics, metabolomics, physical and geochemistry, biochemistry, and cosmochemistry. This scientific community has taken giant strides in understanding the chemistry of life in the past 60 or so years, and has arrived at a place where the limits to life are far beyond those that were previously imagined. Although progress has meant a fundamental re-working of scientists’ understanding of life, they are excited. Astrobiology, the new field in which these scientists unite, faces a great challenge and an even greater frontier: How far can the limits to life be expanded, and how widely in the universe can they be applied?
Acknowledgement
James Scott (1961-2010), former professor of Earth Sciences at Dartmouth College
If there is one thing that I learned from James in the two years that we worked together, it was to appreciate the synergy and intricacy of complex systems. These systems ranged from organic solutions in our lab to theories on the origin of life, and it was only with James’s guidance that I could ever think so scientifically, holistically, and radically about them. This was an effect that James had not only on me, but also on each and every one of his colleagues. James had a rare and striking ability to see connections where no one else did, and to ask questions where no one else ever even thought to ask. This is why, as a scientist, he was truly revolutionary. This is why, as an astrobiologist, he managed to turn the current theory of pressure as a limit to life on its head. And this is why, as a professor, he taught me what kind of scientist I could, and should, strive to be. For this, I could not ever possibly be more grateful. Thank you, James Scott, for showing me, and for showing so many others, a new and beautiful way to think about this world.
References
1. M. D. Guilio, The universal ancestor was a thermophile or a hyperthermophile: Tests and further evidence. Journal of Theoretical Biology 221(3):425-36 (2003).
2. G. Antranikian, Extremophiles, Nature encyclopedia of life sciences. London: Nature Publishing Group (2001).
3. D. G. Burns, P. J. Hanssen, T. Itoh, M. Kamekura, A. Echigo, M. L. Dyall-Smith, Halonotius pteroides, an extremely halophilic archaeon recovered from a saltern crystallizer in southern Australia. International Journal of Systems Evolution Microbiology (2009).
4. P. R. Binks, Radioresistant bacteria: Have they got industrial uses? Journal of Chemical Technology & Biotechnology 67(4), 319-322. (1999)
5. Z. Gengxin, D. Hailiang, X. Zhiqin, Z. Donggao, Z. Chuanlun, Microbial diversity in ultra-high-pressure rocks and fluids from the Chinese continental scientific drilling project in China. Applied & Environmental Microbiology 71(6), 3213(15). (2005).
6. Y. Yano, A. Nakayama, K. Ishahara, H. Saito, Adaptive Changes in Membrane Lipids of Barophilic Bacteria in Response to Changes in Growth 64, 2, 479-485 (1998).
7. F. Abe, C. Kato, K. Horikoshi, Pressure-regulated metabolism in microorganisms, Trends in Microbiology 7, 11, 447-453 (1999).
8. F. Palhano, D. Foguel, G. G. Lindsey, P. Fernandes, Changes in Transcription and Protein Profile Induced by High Hydrostatic Pressure Treatment in Micro-Organisms, Current Proteomics 5, 2, 138-145 (2008).
9. A. Sharma, S. Ruper, J. Scott, Viability of E. Coli cells at deep Earth conditions, submitted to Science (2010).
10. W. S. Reeburgh, D. T. Heggie, Microbial methane consumption reactions and their effect on methane distributions in freshwater and marine environments. Limnology and Oceanography 22, 1-9 (1977).
11. C. Liu, Y. A. Gorby, J. M. Zachara, J. K. Fredrickson, C. F. Brown, Reduction kinetics of fe(III), co(III), U(VI), cr(VI), and tc(VII) in cultures of dissimilatory metal-reducing bacteria, Biotechnology and Bioengineering 80(6):637-49 (2002).
12. A. J. Muller, D. Schulze-Makuch, Thermal energy and the origin of life, Origins of Life and Evolution of Biospheres 36(2). (2006).
13. G. Wanger, Stars of the terrestrial deep subsurface: A novel ‘star-shaped’ bacterial morphotype from a south african platinum mine, Geobiology (2008).
14. L. Lin, P. Wang, D. Rumble, J. Lippmann-Pipke, E. Boice, L. M. Pratt, B. Sherwood Lollar, Long-term sustainability of a high-energy, low-diversity crustal biome, Science 314(5798):479-82 (2006).
15. B. Sherwood-Lollar, Life’s chemical kitchen, Science 304:972-3 (2004).
16. A. Brack, Life in the solar system, Advances in Space Research 24(4):417-33 (1999).