by © 1998 by Werner R. Loewenstein.
Used by arrangement with Oxford University Press, New York.
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Editor's note: The question posed in Werner R. Loewenstein's The Touchstone of Life is, How does living matter manage to organize itself so precisely, complexly, and efficiently, such that it can both function effectively and sustain itself in the face of chaos? In other words, how has life as we know it come to be? The answer, Loewenstein tells us, lies in information: "Information flow, not energy per se, is the prime mover of life. . . . molecular information flowing in circles brings forth the organization we call 'organism' and maintains it against the ever-present disorganizing pressures in the physics universe. So viewed, the information circle becomes the unit of life." Loewenstein pursues his argument by applying what he calls the "strong loupe of information theory" to molecular biology. With this method he reveals the beauties and intricacies of the myriad webs of communication that bring form from formlessness.
Here, Loewenstein provides a précis of how this communication system evolved from its cosmic origins, and explores the molecular dilemma of information conservation versus information transfer.
The Oldest Circus on Earth
A thumbnail sketch of the evolutionary scenario:
Some 10 to 20 billion years ago the four elementary forces burst forth from the primordial Unum, starting the cosmic march of organization from energy particles to atoms to molecules. Here on the cooling Earth, that march went on from symmetric molecules to asymmetric ones, ushering in, 4 billion years ago, the first exchanges of information between molecules of complementary shapes, exchanges where information ran in circles, instead of straight lines - the first molecular cybernetic loops.
Such cybernation began in earnest with RNA molecules, asymmetric structures of enough versatility to serve both as one-dimensional information repositories and three-dimensional actors. Successfully looped, such RNAs can seize as much information as the laws of thermodynamics will give them leave to - a "pulling themselves up by their own bootstraps," where the systems as a whole manage to stay always a little ahead of the game.
Thus, RNA begat RNA. In due season, some structures appeared in this world of RNA, which had features complementary to amino-acid groups. These RNAs could serve as adaptors to get information to flow to amino-acid chains, and so the first proteins came into being on RNA as a template. Eventually, some of the proteins, better catalysts than the RNA, took over the three-dimensional actions. The families of RNA molecules - the successful ones at engendering useful proteins along with some which were not so successful - were amalgamated into a continuous RNA band.
Finally, with the development of proteins capable of catalyzing the formation of DNA from RNA (reverse transcriptase), DNA took over the function of information repository, and RNA got relegated to the role of the intermediary it has today.
In that molecular world centered on DNA, loop was added on information loop, as the repository got longer and longer. By the development of adaptors of various three-dimensional forms - RNAs, proteins, sugars - the loops sprouted connecting branches, forging a huge complex. The complex became twisty and labyrinthine, but all through evolution it maintained its circular shape, for it grew by piling up information circles, more than by piling up information in each circle.
The complex of information loops cuts a spiffy silhouette (figures 1 and 2). But what should one call it? What name is there that would be apt for such an incorporeal something, a circle of circles that rolls through time, grasping more and more information? There is none in our daily language for something so utterly unique, for sure. So I prowled in Greek and Latin dictionaries after a vocable with good roots. I came up with circus where our word circle comes from; circle stems from the Latin circulus, the diminutive of circus. Circus has a nice ring to it and a nice bounce befitting something so alive. But it is its Greek root that will clear away, I think, the hems and haws that naturally crop up with such a neologism. The root is kirkos, which means "ring" and "hawk." This homonym also has enough of Circe rubbed on it, so that - fair warning! - the user is at risk to get smitten with it. Anyway, certainly we will never meet a more rapacious hawk or a grander circus.
The show will go on for as long as the information flows in from the cosmos. But what comes in, must go out - that is the Law - and so the arrow in the logogram on page 116, pointing away from the Circus, rounds out the picture and reminds us that all the hoarded information is but a loan. When the loan comes due in 4 billion years (give or take a few hundred thousand, depending on the temperament of our sun), all those circuli will go back to where they came from. Nevertheless, to those who are inside the Circus, it will always seem the greatest show on Earth, though I can't speak for the One who is outside it.
The Two Information Realms
The Flip Sides of Information: Life's Two Realms
Having discussed how, by means of information loops, a molecular organization might have come out of quantum chemistry, and how, by loop interlacing, such an organization might have pulled itself up in time by its own bootstraps to higher and higher levels, we now take up the information trail in the year 3,500,000,000 post-Circus.
By then that organization has cut its wisdom teeth. The information loops have formed a vast network and the structure materialized has gotten enormously complex. Nevertheless, the guyline of all that information - the linear nucleic-acid structure that serves as a repository - still shines through, and the ancestral division of information depository and temporal expression is as clear as ever.
We might say that information leads a double life: a life in a one-dimensional world where the information is perpetuated in the form of a string of nucleotides, and another in a three-dimensional world where it is acted out in the form of proteins and other structures of a short-lived sort. The information itself, the abstract entity, is the same in either world at a given time; the same entity just appears in different dimensions and uses different makeups. It is a little like making a line drawing and a sculpture of the same subject. Both express similar information, but one is rendered in two dimensions and the other in three. The constraints are
different, though. Whereas the artist has leeway in his expressions and is the better for it, Evolution brings forth hers under the tyrannical rule of equation 3; all her expressions are mathematical transforms, and the only license she is permitted is to choose among random events she does not control.
But why this split of information into separate realms? The answer which most immediately comes to mind is that the split affords a division of function: one realm conserves the information and the other does the work. This is true, but the answer only scratches the surface and smacks of teleology. A twoness that goes through the entire biological sphere is bound to have a more fundamental reason.
So, before we turn to the nitty-gritty of the information flow in organisms, let us wing our way once more out to the origin of life to see the roots of the duality. These can be traced to a fundamental paradox: a conflict between conservation of information and transfer of information. This conflict arose at the very start of the green twig of the cosmic tree, with the first attempts at conserving information by means of organic molecules. That conservation was at loggerheads with transfer of information; such transfer necessarily entails a change in molecular information, a change in molecular structure. Thus, the paradox: if the molecules concerned are absolutely stable, they can't transfer information, and if they transfer information, they can't be absolutely stable.
The evolutionary solution of the dilemma was a Solomonic compromise. The molecular information was partitioned among two realms - one maximizing conservation and the other maximizing the transfer. The two realms were embodied by molecules of distinct structural properties, one kind linear, like DNA, a form that can be easily and faithfully reproduced, and that is stable enough to stay intact in between reproductions, and a second kind three-dimensional, like the proteins, of more temporal and mundane ilk, that can turn over and interact with other molecules. The first kind doesn't do anything; it can't move. And segregated from the other realm, it can be shielded from the ordinary hustle and bustle in the world (in higher organisms the DNA is secluded in the cell nucleus). The second kind can move; impelled by short-range electromagnetic forces, its structure can move between determinate positions and, in turn, set in motion other structures in determinate directions. And the actual mechanical work produced by this electromagnetic pushing and pulling is useful in natural selection; it provides a performance quantity by which the information can be judged in evolutionary competition. [1]
There are several terms commonly in use concerning the two realms "genotype" and "genome," which apply to the conservatory realm, and "phenotype" and "soma," which apply to the three-dimensional realm. These are time-honored names coming from a century of work in genetics. Though not strictly coterminous, they are close enough to the above classification to be considered synonyms of it. However, an unfortunate misusage has crept in in recent years. In the aftermath of molecular biology's triumphal march waving DNA as its banner, it became standing practice to refer to DNA as "the information," reserving this term for that molecule alone. Perhaps that came about because this do-nothing molecule comes closer to the abstract essence of information than the three-dimensional expressions do, or perhaps, because this molecule appears to be the source of information when we look just at a little stretch of the flow, outside the circular context. Old habits die hard, but let's hope that this one proves the exception because such restricted usage of the term obscures the picture. The molecules in both biological realms carry information - an RNA, a protein, or a sugar is as much an informational molecule as DNA is. The quantities they carry individually are different, to be sure, but if we could weigh the total amounts of core information in the molecules of the two realms, they would about balance - the two realms are but the flip sides of the same information.
Werner R. Loewenstein, world renowned for his discoveries in cell communication and and biological information transfer, is director of the Laboratory of Cell Communication at the Marine Biological Laboratories in Woods Hole, Massachusetts.
Endlinks
The RNA World - extensive links to RNA-related online resources.
Study Supports Ancient RNA World - an October 1998 MIT press release describing the discovery of RNA able to catalyze nucleotide formation.
The Beginnings of Life on Earth - summarizes the development of an RNA world hypothesis. From the September-October 1995 issue of American Scientist.
Scientists Debate RNA's Role at Beginning of Life on Earth - focuses on the researchers whose findings have led to this idea. From the March 31, 1997 issue of The Scientist.
Experimental Testing of Theories of an Early RNA World - a more technical look at work in this field. By Andrew Ellington; part of Indiana University's Biotech resource site.
When RNA Ruled: Another Lost World? - HMS Beagle Meeting Brief summarizing recent evidence for an RNA world.
The Origin of Life - HMS Beagle Cutting Edge debate considering what might have been the first living molecular entities.
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