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Crucial Crises in Biology: Life in the Deep Biosphere

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Crucial Crises in Biology: Life in the Deep Biosphere INTERNATL MICROBIOL (1998) 1:285–294 285 © Springer-Verlag Ibérica 1998 REVIEW ARTICLE Ricardo Guerrero Crucial crises in biology: life in the Department of Microbiology, University of Barcelona, Spain deep biosphere Received 25 May 1998 Summary The origin and evolution of life on Earth are the result of a series of crises Accepted 30 June 1998 that have taken place on the planet over about 4500 millions of years since it origi- nated. Biopoiesis (origin of life), ecopoiesis (origin of ecosystems) and the first ecosystems (stromatolites and microbial mats), as well as eukaryopoiesis (origin of nucleated cells) are revised. The paper then focuses on the study of the deep bios- phere, describing ecosystems never found before, which are independent of solar radi- ation and have changed previous assumptions about the requirements of life; even the concept of biosphere, as Vernadsky defined it, has increased its scope. Since the dis- covery, in 1987, of bacteria growing in the crevices of rocks at 500 m deep, in bore- holes drilled near the Savanna River, Aiken, South Carolina, other bacteria have been found in the deep subsurface reaching depths of about 3 km (e.g., in the Columbia River Basalt Group, near Richland, Washington state), in an anaerobic, hot, high-pres- sure environment. Some kinds of microorganisms can thrive at such depths, living in many cases a geochemical existence, by using very specialized metabolisms, which depend on the local environments. The existence of organisms independent from pho- tosynthetic production is the most outstanding, novel feature of the deep biosphere. Living beings might not need other energy and chemical sources than those which occur in the development of all planetary bodies. Life, therefore, could even be an Correspondence to: ineluctable outcome of planetary evolution and, as a corollary, a natural continuation Department of Microbiology. of the usual development of physical phenomena in the universe. University of Barcelona. Av. Diagonal, 645. 08028 Barcelona. Spain. Tel.: +34-934482373. Fax: +34-933341079. Key words Biopoiesis · Ecopoiesis · Stromatolites · Microbial mats · Deep-biosphere E-mail: [email protected] microbiota time. Nevertheless, if life did originate also on them, for some Introduction reason it became extinguished at some later moment. 2. Origin of ecosystems (ecopoiesis). The establishment of In the medical language, crisis is any sudden change, for better a kind of life that fed on the chemical compounds present on or worse, in an acute disease or infection; a sudden exaltation the Earth surface would have had a limit. With the repletion of of the phenomena typical of a chronic disease; or a paroxysmal nutrients—which would have happened in less than 300 million attack of pain, distress or disordered function. Life on Earth is years, life would have become extinguished. It was the not actually a disease, even though we humans may seem to establishment of trophic chains, in which the products of some be bent on making it a serious one. The origin and evolution organism’s metabolism became nutrients for others, that made of life on our planet, however, are the result of a series of crises it possible for life to persist. Over the first two billion years of which have made the Earth and the organisms which live on it evolution, bacteria were the only inhabitants of the planet; they undertake fundamental changes throughout time. I am “invented” most metabolic strategies that exist nowadays. In considering here three turning points, which turned out to be fact, prokaryotes are the only living beings that can be found crucial for the evolution of life. in any kind of habitat, no matter how inhospitable it may be. 1. Origin of life (biopoiesis). It is possible that life originated 3. Origin of eukaryotic cells (eukaryopoiesis). The first around 3800 million years ago. By then, the Earth, which had living beings were prokaryotes; they lacked a nucleus originated 4550 ± 20 million years ago, was ready to shelter differentiated from the cytoplasm, where their genetic material life. It already had liquid water—an essential factor for the was dispersed [17]. Life might have persisted that way. In fact, existence of life—, and a suitable temperature. The bacteria are the only organisms that are not dependent on others characteristics of the Earth’s neighbor planets—Mars and for their survival; on the contrary, they are actually necessary Venus—could have also made the origin of life possible at that for the survival of other living beings. But the level of 286 INTERNATL MICROBIOL Vol. 1, 1998 Guerrero complexity reached in the evolution of bacteria would have establishment of an entity separated from the environment by a been limited. Humans, for example, are the result of an boundary, and being able to both maintain itself actively and evolutionary process that lasted for over 3500 million years, autoreplicate. Such a system is known as autopoietic [21]. and the path leading to our species started when eukaryopoiesis Nor has yet been elucidated when life originated on Earth, took place. Symbiosis was an essential evolutionary mechanism although we have advanced a lot in this quest over the second half in the origin of the eukaryotic cell. of the 20th century. Until the 1950s the story of life before the Cambrian was a mystery. Most paleontologists believed that the earliest organisms on Earth had been soft-bodied single-cell Biopoiesis: the first living beings animals, probably direct ancestors of the trilobites, some worms and other animals which dwelt on the bottom of the oceans and Life is a phenomenon that may have occurred many times and at were very abundant in the early Cambrian [4]. In the 1950s, different places in the universe, provided some circumstances Australian geologist Martin Glaessner found a rock sequence that coincided. Liquid water is a prerequisite for the presence of any did not show the Cambrian/pre-Cambrian discontinuity that had kind of life. When the Earth originated, its surface temperature been usually observed in most locations worldwide. Below the must have been too high for the existence of liquid water. Most Cambrian rocks, Glaessner found well preserved impressions left water presumably escaped to the outer space. The frequent in sand or mud by soft-bodied marine animals of what has been collisions of comets with our planet, once the Earth had cooled, called Ediacaran fauna, because he found them in the Ediacaran may have been responsible for the later presence of liquid water Hills of the Flinders Mountains in South Australia. (Currently [6, 25, 26]. Some 3.9 billion years ago, the Earth must have these organisms are considered to be either protists or lichens, reached a condition compatible with the existence of life. The and there is a tendency to call them Edicara microbiota.) A fossil mechanisms that led to the origin of life have not yet been collector, R. C. Sprigg had already described some of those fossils elucidated, even though the study of the origin of life has made in 1947, but regarded them as being early Cambrian, because at great advancements over the second half of the 20th century. those times it seemed impossible that there would be large fossils Currently we know that, starting from such simple compounds older than those from the Cambrian [10]. Later on other remains as water, NH4 and CO2—all of them present on the Earth in the of Ediacaran fauna were found in England, Greenland and Siberia. Archean period—, and through electrical discharges or ultraviolet In the mid 1950s, another finding showed the presence of microbial radiation it is possible to obtain organic compounds spontaneously. life in rocks two billion years old in the Gunflint Iron Formation, A series of famous experiments carried out in 1953 by Stanley Ontario and northern Minnesota. Paleontologists Elso S. L. Miller [23], by then a twenty-three year old graduate student Barghoorn, of Harvard University, and Stanley A. Tyler, of the of Harold C. Urey (Chemistry Nobel Prize winner in 1934 for University of Wisconsin, found an abundant microscopic life in his discovery of deuterium in 1932), produced the amino acids those sediments, with some forms that resembled some modern alanine and glycine as well as other organic compounds by the bacterial cells [36]. Later studies revealed the presence of fossil action of electrical discharges on a mixture of water, CH4, H2 and bacteria in all rocks studied older than 2000 million years. The NH4. This breakthrough was the beginning of a new discipline, oldest microfossils were found in Warrawoona, Western Australia, which has been known as prebiotic chemistry ever since. Another by Stanley M. Awramik, of the University of California at Santa key discovery was the production of adenine (H5C5N5) from Barbara. Awramik, along with the Precambrian Paleontology hydrogen cyanide (HCN) by Joan Oró in 1959 [26]. Adenine is Research Group directed by J. W. Schopf, of the University of the main component of one of the universal nucleotides which California at Los Angeles, described fossilized bacteria about make up DNA, RNA and ATP. Note that cyanide, a most 3500 million years old, very complex in form, that looked like poisonous substance to humans, which blocks the capacity of some present-day cyanobacteria. Their complexity suggested that hemoglobin to carry oxygen, can also be the source for adenine, life should have already existed for a long time before they were a compound indispensable for life. The primordial broth, abundant laid down in those sediments. Later studies carried out on the in energy-rich organic compounds, could have accumulated oldest known rocks—the 3900 million-year old Isua Formation without oxidizing in the reducing early atmosphere of Earth. in Greenland—did not reveal the presence of cells.
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