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The First Four Billion Years

1999; Cell Press; Volume: 98; Issue: 6 Linguagem: Inglês

10.1016/s0092-8674(00)81488-9

1097-4172

André Brack,

Origins and Evolution of Life

The Molecular Origins of Life: Assembling Pieces of the Puzzle By André Brack Cambridge: Cambridge University Press (1998). 417 pp. $85.00 (hard), $34.95 (paper) The Touchstone of Life: Molecular Information, Cell Communication, and the Foundations of Life By Werner R. Loewenstein Oxford: Oxford University Press (1999). 366 pp. $30.00 The Origins of Life: From the Birth of Life to the Origin of Language By John Maynard Smith, Eörs Szathmáry Oxford: Oxford University Press (1999). 189 pp. $25.00 These are three very different books. The Molecular Origins of Life, edited by André Brack, is a straightforward collection of essays intended for a strictly academic audience. Brack rounds up many of the usual (expert) suspects to summarize what we know, or would like to know, about the earliest history of life on earth. There are chapters devoted to each of the key topics: the early atmosphere (maybe reducing, maybe not); prebiotic synthesis (conceivably terrestrial, but more likely extraterrestrial due to bombardment by comets and micrometeorites); early metabolism (surface-catalyzed iron-sulfur chemistry and thioesters might be important, synthesis of membrane lipids is still problematic, the precursor of RNA-based genetic systems—if indeed there was one—is still unknown); discrepancies between the paleobiological record and phylogenetic deductions (paleobiology will always be the “court of last resort” because it generates hard evidence and hard numbers); and last, but not least, the search for extraterrestrial life (this is the ultimate control experiment—why did life evolve on earth but not on Titan, Saturn's largest satellite, or Mars where conditions may have been almost right?). The Molecular Origins of Life is not full of surprises, but it is a good reference book for those seeking down-to-earth up-to-date facts and theories without a trace of popular hype. As a disinterested molecular biologist, and an avocational contrarian, I was especially amused to read in the chapter by Stanley Miller that deep sea thermal vents—often portrayed as the cauldrons of life—are so hot that any useful organic compounds would almost instantly be destroyed by the heat (“submarine vents do not synthesize organic compounds, they decompose them”). The Origins of Life by John Maynard Smith and Eörs Szathmáry is a superb read—expansive in scope, rich in ideas, light in touch, admirably brief, and equally appealing to lay readers and hard-nosed professionals. The subtitle “From the birth of life to the origin of language” provides ample warning that the authors are either brave or foolhardy, wise or simple. Happily, the authors are brave, wise, and also gifted teachers. Once every few pages, I had to put the book down and let the full implications of a new idea sink in. One of my favorite new ideas emerged in the discussion of the Just-So-Stories we tell ourselves to explain how the urkaryote got its organelles. One problem with the usual endosymbiont hypothesis is that “before a symbiont producing ATP would be of any use to its host, some means of transporting ATP across the symbiont membrane would be needed” (p. 77). Smith and Szathmáry go on to explain that no such difficulty arises with the proposal of Martin and Müller (1998) that the original eubacterial endosymbiont generated H2 and CO2 which could be metabolized by an archaeal host. The obvious virtues of this scheme are that gaseous nutrients would freely diffuse from endosymbiont to host, finessing the need for a transport system, and an archaeal urkaryotic host would explain why eukaryotic information-processing machinery looks more archaeal than eubacterial. This critique of the conventional endosymbiont hypothesis illustrates one of the virtues of the book. Whether the authors are right or wrong, it is almost always fun to watch them thinking and wondering out loud, venturing hypotheses instead of pontificating, and trying to make sense out of this amazing universe we live in (“It is pleasing when peculiar and otherwise baffling facts such as these make sense in terms of a theory that was developed in ignorance of them” [p. 92]). The joy of thinking is particularly evident in the wonderful chapters on “The origin of sex” (geneticists have yet to agree on why sex is good for us), “The origin of many-celled organisms” (“multicellular organisms never have single-celled descendants” because there is “no way back”), and “The origin of language” (“It is especially lucky that eyes of intermediate levels of complexity still exist in animals; reconstruction of the evolutionary history of the eye is an easy task compared with that of the 'language organ': language not only does not fossilize, but there are no living intermediate forms either.” [p. 154]). On the other hand, it must be said that a few chapters—for example, the ten brief pages entitled “From the RNA world to the modern world”—are not strong, but it is the scope and tone of this book, not the bare facts, that recommend it. The Touchstone of Life: Molecular Information, Cell Communication, and the Foundations of Life by Werner R. Loewenstein is a very ambitious book, but the beauty of the central insight—the fundamental equivalence of Shannon's definition of information and Boltzmann's definition of entropy—is marred by purple prose, longwindedness, and a fatal compulsion to develop a Theory of Everything. Ironically, the delightfully slim volume by Smith and Szathmáry, also under review, is a deliberate popularization of a much longer take-no-prisoners academic treatise by the same authors (The Major Transitions in Evolution, 1995). My recommendation is that Loewenstein take a cue from Smith and Szathmáry, and rewrite his ponderous, almost unreadable tome as a brief inspirational volume—perhaps entitled Information Flow in Living Systems—patterned in style and spirit on Schroedinger's What is Life? The barely elaborated central insight would be more powerful if room were left for each reader to apply the new viewpoint to his or her own favorite biological problems. Instead, Loewenstein attempts to have the very last word on every possible topic. I started to count pages. Less can be more. The book is hard to summarize. I will begin with a gripe, move on to some praise, and conclude with another gripe. The first gripe concerns the writing. In contrast to the unremarkable academic prose in The Molecular Origins of Life, or the simple transparent prose in The Origins of Life, The Touchstone of Life is written in a strange amalgam of perfect colloquial English and Old High German. Some of the more distracting hybrids were: “An old clung-to notion thus was stung to the quick” (p. 43). “If we look through a higher lens, we see where the shoe pinches the toe” (p. 98). “What about errors? Their lack hits one still more in the eye than the lack of ambiguity” (p. 145). Although I am as willing as the next fellow to wade through thick swamps of prose to discover the dark secrets of the intellectual jungle, I often found myself in over my head: “It is that that (sic) one may hope one day to find the stationary states which are giving the slip to the present unifying physics theories, the states which may allow us to understand whatever it is that underlies the very nature of matter—all matter, including the biological one. Alas, it may take a while until that unifying sermon will be preached on the streets of Gotham” (p. 333). Overreaching for lively prose can also have impolitic consequences. For example, Loewenstein introduces a metaphorical character called “Lady Evolution” (evolution may be female, but she is certainly not a lady) and entitles a subsection of the book “The Mistress We Can Live Without” (the mistress, it turns out, is none other than Teleology personified). As Auden said of one of his early poems, “It would have been bad enough if I had ever held this wicked doctrine, but that I should have stated it simply because it sounded to me rhetorically effective is quite inexcusable” (Foreword to the Collected Shorter Poems, 1927–1957). Now for the praise. Loewenstein argues that we should try to resee all living systems and indeed the entire biosphere not as the conventional flow of thermodynamic (Gibbsian) free energy, but as the flow of information. And by information Loewenstein decidedly does not mean anything as pedestrian as the mere genetic information that flows from DNA to RNA to protein. Instead, Loewenstein begins by pointing out that Shannon's classic definition of information I = Σ pi log2 pi (where pi refers to the number of subsets of the system) and Boltzmann's definition of entropy S = −k Σ pi ln pi (where k is Boltzmann's constant in calories/°C) differ only by a scaling factor and a sign. Thus I and S are flipsides of one reality: information is a measure of order (which living systems accumulate and transmit), entropy a measure of disorder (the price living systems pay for staying alive), and both I and S can be quantified by describing the distribution of the components of the system over the states available to it. The big question is, How far can you take the notion of information in biology before the notion starts taking you? Loewenstein's thesis echoes the criticism of Watson and Crick (quintessential molecular biologists) made by Barry Commoner (ever the integrative biologist) in the pages of Nature more than 30 years ago (Commoner, 1968). In response to widespread claims that DNA was the “master molecule” of life, containing all the information required to build another cell, Commoner countered with ancient wisdom, going back to Virchow, that only preexisting cells give rise to new cells. DNA means nothing without a preexisting cell to interpret and replicate it. Admittedly, molecular biologists at that time tended to view cells as the grand result of an elaborate self-assembly process, not unlike assembly of bacteriophage particles. In this sense, the existence of genetically encoded macromolecular parts was nearly tantamount to assembling a living whole. Commoner defended a more inclusive definition of genetic inheritance, embracing cellular architecture and the intracellular flow of molecules as equally legitimate, albeit nondigital, forms of genetic information. In a nutshell, DNA replicates but cells do too, and just as it takes DNA to make more DNA, so it takes a cell to make another cell. Q.E.D. Cells must contain other forms of information besides DNA. Although much of the quantifiable information in cells may at first appear to be static (especially cell architecture as glimpsed through the microscope) almost all of this information, except the actual sequence of DNA, corresponds to continual motion: macromolecules moving every which way, small molecules establishing gradients, ions flowing, G proteins undergoing conformational changes in response to GTP hydrolysis, transmembrane receptors changing oligomerization state in response to ligand binding, etc. Similarly, subcellular structures are constantly rearranging, dissolving, and reassembling. One has only to think of vesicle traffic between lamellae in the Golgi stack, cell movement in response to cytokines, or assembly and disassembly of the mitotic apparatus. Loewenstein rightly argues that all of these states of the living system are information-rich; moving between states rearranges or creates information while consuming energy and generating entropy. Three major areas where an informational rather than a Gibbsian view of life may be particularly apt are transcriptional regulation, signal transduction, and cell cycle progression. Combinatorial control of transcription, cross talk between signaling pathways, and cell cycle checkpoints are often described in the literature—borrowing the language of computer science—as integrative (perhaps integrated!) circuitry, able to combine many diverse inputs into a single practical output. This is biological computing at its best, and Loewenstein argues that macromolecular switches (G proteins for example) and microelectronic switches (transistors on the motherboard) are fundamentally similar. In each case, the switch exists in two (or more) states; switching back and forth between states consumes energy and generates entropy, while transmitting or creating information. My second gripe is more serious. Although the two states of a G protein may formally resemble a transistor in action, the nature of the information storage, and the detailed thermodynamics of the two states, are profoundly different: one switch is a macromolecule composed of 3,000 covalently attached atoms, the other is a microscopic sandwich with a handful of electrons moving through a doped silicon wafer. Similarly, a wave of depolarization traveling down an axon may be formally analogous to electrons flowing through a copper wire, but the physical nature of these two processes is so different that the analogy does not readily suggest new biological experiments or new theories of neural function. Apparently, there is little in biology that cannot be formally viewed in terms of the acquisition, maintenance, replication, transmission, and degradation of information. This allows Loewenstein to bend much of biology to his purpose, exploiting the information metaphor as a rhetorical device to construct popular accounts of many interesting tales in modern biology. The metaphor is often invigorating, but it does not seem to be intellectually or experimentally useful in the long run. As Smith and Szathmáry put it in The Origins of Life, “The point of analogies of this kind is not that they are true but that they suggest questions to ask, and predictions to test” (p. 106). Loewenstein's insistence on viewing all of nature as the flow of information ultimately fragments biology instead of unifying it. The natural world cannot be fully appreciated through a kaleidoscope. References Auden, W.H. (1966). The Collected Shorter Poems, 1927–1957 (New York: Random House), p. 15. Commoner, B. (1968). Nature 220, 334–340. Martin, W., and Müller, M. (1998). Nature 392, 37–41. Alan M. Weiner a aDepartment of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, Connecticut 06520-8024