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Journal of Biological Physics 20: 3-9, 1994. 1995 KluwerAcademicPublishers. Printedin the Netherlands.

THE ORIGIN OF THE CELL FROM OPARIN TO THE PRESENT DAY

CYRIL PONNAMPERUMA Laboratory of Chemical Evolution University of Maryland College Park, Maryland 20742, U.S.A.

I ask the question, Why was it that Oparin made such a difference? Perhaps the answer lies in the fact that Oparin was an unusual scholar. He looked upon a problem that was philosophical in essence, but brought to bear upon it history and all science. His writings referred liberally to the philosophy of Aristotle of ancient Greece and to the work of the christian savant Augustine, and yet he also described in detail the scientific work of Louis Pasteur. Although a biochemist by training, Oparin moved freely from astronomy to chemistry, from geology to biology, with the thread of philosophy woven throughout. Oparin demonstrated an insight into the writings and teachings of the philosophers. After the collapse of the theory of spontaneous generation following Louis Pasteur's epoch-making experiments, the concept of life as eternal, with changes only in form, came back to the fold. Oparin in his analyses points out that the same vitalistic concept, the same dualism, was at the bottom of the theory of the continuity or eternity of life. The "Actus Dei" of Augustine, the "Entelechy" of Aristotle, the "Spiritus Vitae" of Paracelsus, the "Archai" of Van Helmont - no matter what form the theories of the continuity of life assume, they always leave an unbridgeable gap between the kingdom of organisms and inorganic nature. Oparin was able to demonstrate by his analyses of this philosophical thought that there was another path to follow. We have followed such a path. It is Oparin who gave us the idea of the continuity in the universe from the inorganic to the organic, from the elements to the small molecules. The concept of cosmic evolution, then, comes to us from his early writings. In a way, he personified the student of chemical evolution as described by J. D. Bernal, who said that "Even the formulation of this problem is beyond the reach of any one scientist. Such a scientist would have to be at the same time a competent mathematician, physicist, and experienced organic chemist. He should have a very extensive knowledge of geology, geophysics, and geochemistry, and besides all this be absolutely at home in all biological disciplines." What Bernal wrote in 1948, Oparin had already revealed to us in the '20s. Since it is difficult to find a single person competent in all disciplines, we bring a group together, different people who will interact and then put their knowledge together. It was Oparin who, in 1957, organized the first international conference on the

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origin of life. That meeting established a pattern for study of the subject by having been organized under the auspices of the International Union of Biochemistry. Oparin was there as the host and organizer. It was my great pleasure to later have met Alexander Ivanovich Oparin at the Wakulla Springs Conference in 1963, convened by Sidney Fox. That conference was another landmark gathering. Also attending was another great thinker in the field, J.B.S. Haldane. To those of us who at that time were groping our way through the first steps of chemical evolution, however, Oparin stood out as a giant. NASA had begun its work on exobiology, and the National Academy of Sciences of the United States had declared the search for extraterrestrial life a prime goal of space biology. Great activities sprung up from many angles, ~pecially in relating the origin of life to the possible existence of life beyond the Earth. Oparin's work now began to have a cosmic implication. From Wakulla Springs we move to our next highlight in this sequence of important conferences - Cortina D'Ampezzo. Sidney Fox and I were once again privileged to be part of this special conference on the origins of life. It was here, at Cortina D'Ampezzo, in Oparin's hotel room looking out at the dolomites and in this wonderful atmosphere, that the International Society for the Study of the Origin of Life (ISSOL) was bern. Oparin was its first president, Sidney Fox its vice president, and your humble servant its secretary. Alas, today many members of this society, which now numbers over 500, hardly know its beginnings or the fact that it was Oparin himself, egged on by Sidney Fox, who felt the time was right to bring together from all over the field these different researchers. From there Alexander Ivanovich Oparin traveled widely. He went to NASA's Ames Research Center in California. There he lectured to groups and continued his interaction with young people, activities that he devoted much time to over the years. In 1977, after the Viking landing on Mars, the famous meeting in Kyoto was held. One might say that at that meeting Oparin had truly reached the pinnacle of his international stature. ISSOL decided to establish a medal in his honor, to be awarded every three years for the most meritorious scientific work on the origins of life. From a scientific point of view, possibly the greatest contribution Alexander Ivanovich Oparin made to the study of the origins of life was his careful analysis of the nature of the primitive atmosphere. He suggested that the carbides in the crust of the Earth may have given rise to hydrocarbons. Indeed, the carbides may have come from meteorites, and it is interesting now for us to combine some of this thinking. (The presence of hydrocarbons in meteorites was established by Wohler when he analyzed a piece of the Kaba.) Here, then, was a source of the reduced carbon necessary for the organic molecule. Oparin also argued that in the amino acids the carbon and nitrogen are in the reduced form and that, therefore, the starting materials may have been in that form. This was a remarkable proposition to make at the time, of course, knowing as we do now the amount of time and trouble in the laboratory it has taken students since then to arrive at the same conclusion. (It was Harold Urey who showed at that time the reduced nature of the primitive atmosphere.) Much of the work being done at the time was therefore being done as a result of this early hypothesis Oparin put forward almost

THE ORIGIN OF THE CELL FROM OPARIN TO THE PRESENT DAY

Alexander Ivanovich Oparin and Cyril Ponnamperuma at the Cortina D'Ampezzo conference

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intuitively - not by the study of equilibrium data, but simply by his contact with the carbides and his understanding of the composition of amino acids. He realized that the amino acids must have had reduced nitrogen, and so he argued for the reduced nature of primitive materials. As a matter of fact, Oparin concentrated a great deal on the possible role of the CN fragment. This is also remarkable, considering what we now know of organic chemistry as related to chemical evolution. In 1961 John Ore used ammonium cyanide to produce adenine. In the work that has been done since then, we have realized that the role of cyanide plays an important part in the prebiotic synthesis of the generation of amino acids from the nitrile. So Oparin's insight into that fragment, the CN fragment, which he postulated as important, is indeed remarkable from our point of view. Radio astronomers have now observed nitriles and hydrogencyanide in the interstellar medium. While emphasizing the need to study the chemistry of cyanide molecules, Oparin realized that fundamentally the main question had to do with organization. According to him there were at first the simple solutions of organic substances whose behavior was predicated by the properties of their component atoms and the arrangement of these atoms in the molecular structure. But gradually, as the result of the growth and increasing complexity of the molecule, new properties were emerging, and a new colloidal chemical order was imposed on the simplest organic chemical reaction. So here we get the first hints that Oparin was studying self-organization. According to him, the new properties were determined by the spacial arrangement and mutual relationship of the molecules. In this process biological order is already coming into prominence. Taking his cue from the Dutch physical chemist, Bungenberg de Jong, Oparin looked at the formation and concentration of materials from diluted solutions. He realized that coacervates could easily be contained under laboratory conditions by the simple mixing of a solution of different proteins and other substances of high molecular weight at ordinary temperatures and, in most cases, with very little acidity. Molecules that were previously distributed throughout the medium would now come together in coacervate formation. Then our components would attract one another, and at a pretty low concentration would collect in the liquids to form swarms or clumps that would separate them from the solution until they reached a particular size. They would appear to be very well defined. Indeed, here are the coacervates of Oparin's that could have been forerunners of modem cells. In his monumental studies on the coacervate droplets, Oparin showed that they could have internal structures different from those found in simple droplets of liquid. In a series of very comprehensive experiments, he showed how easily these reactions could take place within the coacervate. Indeed, in some experiments he showed how enzymatic reactions could be possible. The whole school of Russian scientists who work on coacervates owe their knowledge and background to the first experiments of Alexander Ivanovich Oparin. He argued further that from these molecules, complete multimolecular systems could have been formed. Oparin's reflections on the origins of life led him to examine the possibility of life beyond the Earth. He postulated that the conditions suitable for the origins of life had

THE ORIGINOF THE CELLFROMOPARINTO THE PRESENTDAY

existed on the primitive Earth, but that the primitive Earth was only one o f many suitable locations in the universe. Modern astronomy, of course, tells us that there are billions and billions o f sites in the universe where life is possible. So from that one successful experiment on the Earth, we can turn to places elsewhere in the universe. Astronomers tell us that there are 10~3 stars in the universe. To us chemists, that is a happy number - the Avogadro number. If we take a conservative estimate, 1 percent of these Stars can have around them conditions suitable for life. We are still talking about a colossal number - 10:~ possibilities. Planets are plentiful in the universe. Oparin's model o f the primitive Earth can be extended elsewhere in the universe. We have just celebrated the 25th anniversary o f the lunar landing. Oparin was with us in California when that magnificent event took place. Soil samples were brought back to the laboratory, where Sidney Fox, John Ore, myself and others proceeded to analyze them. Oparin was one of those most excited about the analysis and what it would possibly reveal to us. The Moon did not show us very much, but then came the meteorites, especially the Murchison meteorite; Oparin had referred in his writings to their possible relevance in origin-of-life studies, primarily going back to what he had read about Wholer and others. Twenty-five years ago, on September 21, 1969, this meteorite fell in Murchison, Australia. We were able to smuggle out a chunk of it. We were preparing for the lunar analysis, and although the lunar samples had not yet arrived, we were able to apply the techniques developed for their subsequent analysis to the Murchison sample. Lo and behold, the Murchison meteorite gave us the first conclusive evidence of extraterrestrial amino acids. Once again, this is another landmark event in the study of the origin of life. Follow Oparin beyond his insight on meteorites to the interstellar medium once again - the organic chemistry that was postulated as primordial now enter the interstellar medium. Then to Mars, where in 1976 the Viking spacecraft landed. The reason I mention this is because there was a very close relationship between some of Oparin's thinking and the possibility of life on Mars. Remember, Oparin looked upon the Earth as one example of a laboratory. The first opportunity for us to test the hypothesis of the evolution of life was on Mars. If there was life on Mars and we could demonstrate its independent origin, then certainly we would have unquestionable evidence o f the possibility of life elsewhere in the universe. For Mars we had one set of experiments for the organic analysis, the GCMS, and another for biology. The experiments conducted were simple ones: the gas exchange, the label release, and the pyrolytic release. The whole idea was to take a handful of the soil, expose it to a medium, and see whether life was detected there. Indeed, the results indicated something positive. Even the team leader of the biology experiment, Chuck Klein, concluded that the biology experiments, if taken alone, would indicate that there was life on Mars. But then came the GCMS. The GCMS experiment indicated that there was less than 5 parts per billion o f organic matter. It was then our task to point out that this was i n d e ~ the surface of Mars mimicking biology. Inorganic analysis had indicated to us a composition of the Martian surface, and in our laboratory we had a tube containing simulated surface. Upon examination we found that the ironoxide on the

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surface of Mars, when exposed to ultraviolet light, behaved just as though it were biological. The paper we published in Science that year on the results of the Viking mission seemed conclusive. Now we have a different story. During the course of our studies, we found that the GCMS used in the Viking mission had also been used to test soil from the Antarctic in which there were microbes. The GCMS could not detect organic matter in the Antarctic sample. This information comes to light only now. We have therefore requested NASA to impound the two model prototypes that are available: one at Jet Propulsion Laboratory and one at the Smithsonian. They will soon come over to my laboratory, where they will be retested. The understanding is very simple: A single microbe in the Antarctic soil, from what they call the dry valley, could multiply and give the biology result, but a single microbe could not be detected by the GCMS. So now we have an opportunity to reexamine the Viking findings. In a way, we owe this insight to the early thinking of Alexander Ivanovich Oparin. From Mars we move to the other planets. Voyoger's results have been very prominent recently beeanse of the impact of the Shoemaker-Levy 8 Comet. Voyager gave us a magnificent picture of Jupiter's red spot. Laboratory work showed that organic matter could be produced there. The colors in a photograph of Jupiter are the result of the chemical reactions that will occur between methane and ammonia in highly reduced conditions - Oparin's idea of the primitive atmosphere of any planet. The droplets seen in a photograph of Titan are collections of organic molecules that are there. So in a way, the reducing atmosphere of this planet can be connected to Oparin's early thinking. A 1986 photograph of Halley's Comet does not reveal as much as one from 1910, but in observing its trek we were able to detect the presence of various hydrocarbons, hydrogencyanide, and so forth. We are moving, then, from the idea of the primitive atmosphere of the Earth to the primitive atmospheres of other planets to the general presence of organic matter under interstellar conditions. If this is indeed the case, surely life would have evolved to the point where intelligent life is present elsewhere. In 1960, Frank Drake used the Tatel telescope at the Green Bank Observatory to search for signals from outer space. Unfortunately, the two-month search - named Project Ozma after the Princess of Oz - did not yield evidence of extraterrestrial intelligence. However, Drake's work eventually led to an international program. On October 12, 1992, to commemorate the 500th anniversary of the landing of Columbus in America, NASA launched its ambitious SETI program, the High Resolution Microwave Survey. Unfortunately, the project was cut from NASA's budget the following year. Thanks to the work of private citizens around the world, however, the SETI Institute, with Frank Drake as its president, is now privately funding the continuation of this project. The institute has developed some major proposals, one of which is to act on a recommendation that came out of Project Cyclops, funded by NASA in 1973, to construct a whole array of 10-meter wide antennae that would pick up signals from outer space. A whole range of them placed somewhere without interference - perhaps someday even on the further side of the Moon - would give us knowledge of what is happening out there.

THE ORIGINOF THE CELLFROMOPARINTO THE PRESENTDAY

We come back here, then - after our odyssey from the Earth to the Moon to the meteorites to Mars, to comets to the giant planets to the stars beyond - to the possibility of life beyond. This is indeed an idea that came from that first publication in 1923. One could say that what Darwin is to biological evolution, Oparin is to chemical evolution. Oparin spoke o f the general origins of life. Not as a special event, but as a phenomenon that could commonly take place. And this brings us back to something that is happening on the Earth today. The Earth is the only place where we know there is life. A few years ago, Alvin, the submarine that went down to the bottom of ocean, brought back to us samples from the hydrothermal vents. For almost forty years we had worked in our laboratories on the assumption that the conditions suitable for the origins of life had disappeared. But here we find them. Therefore, we must rationally accept the likelihood that life is arising there now. As a matter of fact, the conditions there are far superior to those in the laboratories at College Park, San Diego, Houston, or Miami. We know there are micro-organisms living under these conditions, even though there is some dispute regarding the actual temperatures. The work of Barros and his colleagues from the San Juan DeFuca hydrothermal vents indicates that microorganisms possibly can exist at 160 degrees centigrade under those conditions, and at about 760 atmospheres of pressure because of the presence of liquid water. So here we have an opportunity to examine what Oparin described as the general appearance of life, that it is not something confined to one place or one time on Earth, but perhaps to the end of the {lnlverse. Of course, each dive of the Alvin costs $5 million. We have been urging NASA, NRL, and the NSF for the last few years to fund such a project because it would give us a unique opportunity to establish the basis of a problem of major importance. Already we have pieces of the vents in the laboratory and are analyzing them in the way we analyzed the meteorites. There is a ray of hope: Thanks to the end of the Cold War, there is now an attempt to use military hardware for peaceful purposes, and we have been able to persuade U.S. Senator Inouye of Hawaii to declare that one submarine be called a "white submarine ~ for science. If the Senate appropriations process underway right now provides the money, we will have an opportunity of taking Alvin down to the bottom of the oceans to study some of these vents. There are, according to the geophysicists, some 40,000 kilometers of hydrothermal vents. We have looked at some of these: the San Juan DeFuca in the area near Seattle, the one in Southern California, and the one at 21 degrees latitude. So here we have an opportunity to verify the idea o f Alexander Ivanovich Oparin, who long ago described as a possibility the general emergence of life. I trust that in these introductory remarks I have been able to give you in small measure what we owe to Oparin, and I hope that with this lOOth anniversary celebration we have had, first in Moscow and now in Trieste, there will be further interest in and enthusiasm for the study of what Oparin began so many years ago.