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A Molecular View of Microbial Diversity and the Biosphere Norman R A Molecular View of Microbial Diversity and the Biosphere Norman R. Pace, et al. Science 276, 734 (1997); DOI: 10.1126/science.276.5313.734 The following resources related to this article are available online at www.sciencemag.org (this information is current as of September 6, 2007 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/cgi/content/full/276/5313/734 This article cites 20 articles, 19 of which can be accessed for free: http://www.sciencemag.org/cgi/content/full/276/5313/734#otherarticles This article has been cited by 97 articles hosted by HighWire Press; see: http://www.sciencemag.org/cgi/content/full/276/5313/734#otherarticles This article appears in the following subject collections: Microbiology http://www.sciencemag.org/cgi/collection/microbio on September 6, 2007 Information about obtaining reprints of this article or about obtaining permission to reproduce this article in whole or in part can be found at: http://www.sciencemag.org/about/permissions.dtl www.sciencemag.org Downloaded from Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 1997 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS. ticularly the multicellular forms. A Molecular View of Microbial The breakthrough that called to ques- tion many previous beliefs and brought or- der to microbial, indeed biological, diversity Diversity and the Biosphere emerged with the determination of molec- ular sequences and the concept that se- Norman R. Pace quences could be used to relate organisms (5). The incisive formulation was reached Over three decades of molecular-phylogenetic studies, researchers have compiled an by Carl Woese who, by comparison of ribo- increasingly robust map of evolutionary diversification showing that the main diversity somal RNA (rRNA) sequences, established of life is microbial, distributed among three primary relatedness groups or domains: a molecular sequence–based phylogenetic Archaea, Bacteria, and Eucarya. The general properties of representatives of the three tree that could be used to relate all organ- domains indicate that the earliest life was based on inorganic nutrition and that pho- isms and reconstruct the history of life (6, tosynthesis and use of organic compounds for carbon and energy metabolism came 7). Woese articulated the now-recognized comparatively later. The application of molecular-phylogenetic methods to study natural three primary lines of evolutionary descent, microbial ecosystems without the traditional requirement for cultivation has resulted in termed “urkingdoms” or “domains”: Eucarya the discovery of many unexpected evolutionary lineages; members of some of these (eukaryotes), Bacteria (initially called eu- lineages are only distantly related to known organisms but are sufficiently abundant that bacteria), and Archaea (initially called ar- they are likely to have impact on the chemistry of the biosphere. chaebacteria) (8). Figure 1 is a current phylogenetic tree based on small-subunit (SSU) rRNA se- quences of the organisms represented. The Microbial organisms occupy a peculiar was not until the late 19th century and the construction of such a tree is conceptually place in the human view of life. Microbes development of pure-culture techniques simple (9). Pairs of rRNA sequences from receive little attention in our general texts that microbial organisms could be studied as different organisms are aligned, and the dif- of biology. They are largely ignored by most individual types and characterized to some ferences are counted and considered to be professional biologists and are virtually un- extent, mainly by nutritional criteria. How- some measure of “evolutionary distance” be- known to the public except in the contexts ever, the pure-culture approach to the study tween the organisms. There is no consider- of disease and rot. Yet, the workings of the of the microbial world seriously constrained ation of the passage of time, only of change on September 6, 2007 biosphere depend absolutely on the activi- the view of microbial diversity because most in nucleotide sequence. Pair-wise differences ties of the microbial world (1). Our texts microbes defy cultivation by standard meth- between many organisms can then be used articulate biodiversity in terms of large or- ods. Moreover, the morphological and nu- to infer phylogenetic trees, maps that repre- ganisms: insects usually top the count of tritional criteria used to describe microbes sent the evolutionary paths leading to the species. Yet, if we squeeze out any one of failed to provide a natural taxonomy, or- modern-day sequences. The tree in Fig. 1 is these insects and examine its contents un- dered according to evolutionary relation- largely congruent with trees made using any der the microscope, we find hundreds or ships. Molecular tools and perspective based molecule in the nucleic acid–based, infor- thousands of distinct microbial species. A on gene sequences are now alleviating these mation-processing system of cells. On the handful of soil contains billions of microbial constraints to some extent. Even the early other hand, phylogenetic trees based on www.sciencemag.org organisms, so many different types that ac- results are changing our perception of mi- metabolic genes, those involved in the ma- curate numbers remain unknown. At most crobial diversity. nipulation of small molecules and in inter- only a few of these microbes would be action with the environment, commonly do known to us; only about 5000 noneukary- A Sequence-Based Map not concur with the rRNA-based version otic organisms have been formally described of Biodiversity [see (10, 11) for reviews and discussions of (2) (in contrast to the half-million de- phylogenetic results with different mole- scribed insect species). We know so little Before the development of sequence-based cules]. Incongruities in phylogenetic trees about microbial biology, despite it being a methods, it was impossible to know the made with different molecules may reflect Downloaded from part of biology that looms so large in the evolutionary relationships connecting all of lateral transfers or even the intermixings of sustenance of life on this planet. life and thereby to draw a universal evolu- genomes in the course of evolution. Some The reason for our poor understanding tionary tree. Whittaker, in 1969, just as the metabolic archaeal genes, for instance, ap- of the microbial world lies, of course, in the molecular methods began to develop, sum- pear much more highly related to specific fact that microbes are tiny, individually in- marized evolutionary thought in the con- bacterial versions than to their eucaryal ho- visible to the eye. The mere existence of text of the “Five Kingdoms” of life: animals, mologs; other archaeal genes seem decidedly microbial life was recognized only relatively plants, fungi, protists (“protozoa”), and eukaryotic in nature; still other archaeal recently in history, about 300 years ago, monera (bacteria) (3). There also was rec- genes are unique. Nonetheless, the recently with Leeuwenhoek’s invention of the mi- ognized a higher, seemingly more funda- determined sequence of the archaeon Meth- croscope. Even under the microscope, how- mental taxonomic distinction between eu- anococcus jannaschii shows that the evolu- ever, the simple morphologies of most mi- karyotes, organisms that contain nuclear tionary lineage Archaea is independent of crobes, usually nondescript rods and membranes, and prokaryotes, predecessors both Eucarya and Bacteria (12). spheres, prevented their classification by of eukaryotes that lack nuclear membranes morphology, the way that large organisms (4). These two categories of organisms were Interpreting the Molecular had always been related to one another. It considered independent and coherent relat- Tree of Life edness groups. The main evolutionary di- The author is in the Departments of Plant and Microbial versity of life on Earth, four of the “Evolutionary distance” in this type of phy- Biology and Molecular and Cell Biology, University of California, Berkeley, CA 94720–3102, USA. E-mail: five traditional taxonomic kingdoms, was logenetic tree (Fig. 1), the extent of se- [email protected] thought to lie among the eukaryotes, par- quence change, is read along line segments. 734 SCIENCE z VOL. 276 z 2 MAY 1997 z www.sciencemag.org ARTICLES The tree can be considered a rough map of from free-living organisms that branch pe- ample of similarities and differences is in the the evolution of the genetic core of the ripherally in molecular trees. Moreover, the nature of the transcription machinery. The cellular lineages that led to the modern most deeply divergent eukaryotes even lack RNA polymerases of Eucarya and Archaea organisms (sequences) included in the tree. mitochondria (15). These latter organisms, resemble each other in subunit composition The time of occurrence of evolutionary little studied but sometimes troublesome and sequence far more than either resembles events cannot be extracted reliably from creatures such as Giardia, Trichomonas, and the bacterial type of polymerase. Moreover, phylogenetic trees, despite common at- Vairimorpha, nonetheless contain at least a whereas all
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