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1 May 2003 EXPLORING EVOLUTION, ECOLOGY, BREEDING, BIOINFORMATICS, AND BIOPRESERVATION
CHRISTINA WALTERS
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Life at the Limits: Organisms in Extreme Environments. David A. Wharton. Cambridge University Press, Cambridge, United Kingdom. 2002. 320 pp., illus. $25.00 (ISBN 0521782120 cloth).

Life at the Limits was a refreshing reminder of why I became involved in biology research. This 320-page book (with 53 illustrations and four tables) describes organisms found living under extreme environmental conditions and—weaving through themes of the nature of life and its ecology, evolution, and origin—discusses the possibility of extraterrestrial life. These are not esoteric questions; studies of life under extreme conditions brought us creamier ice cream, laundry detergent that works in cold water, and other practical innovations. The author of this imaginative and up-to-date survey is David A. Wharton, an associate professor of the Zoology Department at the University of Otago, New Zealand.

The premise of the book is that all living things, no matter how exotic, have the same basic rules, goals, and equipment, but some organisms have specific strategies to cope with severe environmental stresses. These stresses range from extremes in temperature and water availability and pressure to radiation and toxic chemicals. Not surprisingly, Wharton proclaims that the availability of water, specifically liquid water, is key. Research in a number of laboratories, including mine, suggests that the profound requirement for liquid water is based on the fluidity that it provides. If this is true, then even the single requirement for liquid water could be replaced in other worlds by a chemical that provides the proper capacity for molecular movement under strange (at least to us) conditions of temperature, pressure, and composition.

The book would be a good read for anyone interested in biology, but particularly for those wishing to explore evolution, ecology, breeding, bioinformatics, and biopreservation in a broad or unusual context. Biology teachers could use examples from the text to make class more interesting or to demonstrate a fundamental principle. Strategies to cope with extreme environments might also provide perspectives on gene mining (e.g., the Taq polymerase isolated from organisms in hot springs, which profoundly changed biological research), engineering (e.g., lessons from ants on how to build homes that don't cook in the sun), antibioterrorism (e.g., understanding the weaknesses of tough organisms to help defend against them), and exploration (e.g., what to take to remote places and what to expect). Students of the history of science will find the account of the century-long debate on anhydrobiosis (life without water), from the 1750s to the 1850s, an example of the inextricable, long-lived link between humans and the science that they do. Although a biology background is not necessary to get the gist of the book, some scientific knowledge would be helpful, since the text can be technical in places. Even so, I would not recommend this book as a reference source or textbook, because it does not directly cite sources, and in some cases it provides only a single perspective on questions that are still being debated in the literature.

Wharton makes an insightful effort to define the terms extreme and normal and to specify what might be considered stressful. Though he tries to be objective by using the “Life Box” concept, which specifies conditions where most species may be expected to exist, it is clearly a struggle for him to avoid anthropocentricity, and he admits near the end of the book that biases may be inevitable. These potential biases are reflected mostly in the choice of environments that are considered extreme; Wharton proposes that extremity is relative, especially in time, space, and creature. He explains that extreme environments may have been the normal condition of early Earth and that extreme organisms may actually be the vestiges of original populations. The possibility that life evolved from what are now considered extreme environments fuels arguments about whether survival strategies are conserved traits or adaptations.

As a stress physiologist, I thought Wharton's discussion of adaptations (or traits) that enable organisms to survive stressful conditions to be further complicated, because he defines these adaptations or traits in an ecological context in which functional differences among strategies are intermingled. He distinguishes between capacity adaptations, which allow organisms to function (i.e., metabolize, grow, reproduce) under harsh conditions, and resistance adaptations, which enable the organism to avoid the harsh conditions—either by changing the environment, by moving away from it, or by going quiescent and waiting for a rainy day (so to speak). In my field, by contrast, organisms that survive stress, either by remaining active or by shutting off metabolism, are considered tolerant of it. The definition of avoidance strategies, and hence the distinction between capacity adaptations and resistance adaptations, is fraught with ambiguity. Avoiding stress by moving or modifying, for example, requires different structures than does surviving the implicit physical disruptions. To complicate matters further, avoidance can also be a capacity adaptation, as is demonstrated by thermal hysteresis proteins, which provide a mechanism to avoid ice growth in cells (the stress) and which also allow polar fishes to swim at subfreezing temperatures without freezing. These functional distinctions are important to humans who wish to make use of the exceptional qualities of extreme organisms.

The issues of time and isolation, which are scattered throughout the text, are not conclusively reconciled. Wharton suggests that the lichens on his slate roof may be several hundred years old. However, it is difficult to tell the actual age of the organisms. Perhaps there are sufficient capacity adaptations for reproduction, and so, while the population has persisted, the organisms are chronologically young. These questions can be posed for many organisms that are believed to be ancient. Thus, we continually return to the ideas of capacity adaptation versus quiescence, and in this context the nature of metabolism must be sorted out. Minor conditions of radiation, isolation, time, and even fire may actually be the true determinants of organisms' ability to colonize and thrive in new places previously devoid of life.

The book may be most enjoyable when read out of sequence, with chapters 1 and 2 covered first, followed by chapters 7 and 8, and finally chapters 3 through 6. This way, the reader would first be exposed to broad concepts of extremity and places on Earth considered to be extreme and then receive a good overview of general strategies for survival and their prevalence among diverse organisms and stresses. Knowing why “extreme biology” is important (chapter 8) provides a good entry into the middle chapters, which give specific details about organism morphology and behaviors that enable organisms to cope. The style of the middle chapters is a departure from the evolutionary or ecological context used in earlier and later chapters. In these middle chapters, discussions about eukaryotes focus mostly on the animal kingdom, and readers with botanical interests may be disappointed by the brief and very general coverage of the remarkable adaptations of plants that endure extreme conditions.

Life at the Limits provides a fascinating account of life, how precarious it is, and also how resilient. Many of the places the author describes are threatened (“the Dead Sea is dying”). Many of the organisms described are at the limit of their tolerance and will perish if the weather gets colder or dry spells become longer. Many other organisms are tough and opportunistic; these may provide benefits to the human community, such as cleaning up toxic wastes, or may become invasive pests. Organisms living at the limits of survivable space and time tell us about how Earth is and was; they also tell us about the possibilities of life outside Earth's atmosphere. Finally, depending on how we care for this planet, these unique organisms may be the harbingers of future Earth.

CHRISTINA WALTERS "EXPLORING EVOLUTION, ECOLOGY, BREEDING, BIOINFORMATICS, AND BIOPRESERVATION," BioScience 53(5), 524-525, (1 May 2003). https://doi.org/10.1641/0006-3568(2003)053[0524:EEEBBA]2.0.CO;2
Published: 1 May 2003
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