DOCSLIB.ORG

Phylogeny and Beyond: Scientific, Historical, and Conceptual Significance of the first Tree of Life

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Phylogeny and Beyond: Scientific, Historical, and Conceptual Significance of the first Tree of Life PNAS CLASSIC PERSPECTIVE Phylogeny and beyond: Scientific, historical, and conceptual significance of the first tree of life Norman R. Pacea,1, Jan Sappb, and Nigel Goldenfeldc aDepartment of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, CO 80309; bBiology Department, York University, Toronto, ON, Canada M3J 1P3; and cInstitute for Genomic Biology and Department of Physics, University of Illinois, Urbana, IL 61801 Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved December 20, 2011 (received for review November 29, 2011) In 1977, Carl Woese and George Fox published a brief paper in PNAS that established, for the first time, that the overall phylogenetic structure of the living world is tripartite. We describe the way in which this monumental discovery was made, its context within the historical development of evolutionary thought, and how it has impacted our understanding of the emergence of life and the characterization of the evolutionary process in its most general form. fundamental breakthrough in Several aspects of the paper by Woese species and organism and bringing to the biological science occurred in and Fox (1) sparked skepticism. One fore the deep limitations of earlier ac- A 1977, and most biologists did was the arcane nature of the molecular counts of the evolutionary process. not notice. The paper by Woese data, which few could appreciate. The re- and Fox (1) in 1977 was 2.5 pages in length liance on a single gene to trace major Lead Up to the Paper and contained a single table of numbers trends in evolution was an equally alien The 1977 paper by Woese and Fox (1) was that compared sequence snippets derived concept. Some quibbled about the name an early example of what we would today from small subunit rRNAs of different archaebacteria; others objected to The call molecular phylogenetics—the com- organisms. The table provided the first New York Times publicity. Most impor- parison of macromolecular sequences to gene sequence-based quantitative assess- tantly, however, the conclusions of the infer genealogical and thereby, evolution- ment of phylogenetic (evolutionary) rela- paper flew into the face of the common ary relationships. The notion of comparing tionships between representatives of the wisdom of the time regarding the basic sequences to infer relationships was put major known kinds of organisms (1). The divisions of biology and the nature of early forward in 1958 by Francis Crick (3) and paper showed that all cellular life falls into evolution. It was generally believed—and more formally, by Emil Zuckerkandl and one of three large relatedness groups: still is taught in our textbooks—that life Linus Pauling in 1965 (4). This was a eukaryotes (our kind of cells, which con- is of two kinds: on one hand, eukaryotes time when determination of protein se- tain a nuclear envelope), eubacteria and on the other hand, prokaryotes, which quences had become, to some extent, [Woese and Fox (1) termed the group and lack nuclear membranes and as the name tractable with protocols developed by Fred fi this group is where classically studied implies, were supposed to have preceded Sanger (5), who received his rst Nobel bacteria fit], and archaebacteria [an un- and evolved into eukaryotes. However, Prize for that development and the de- usual group of recently described organ- eubacteria and the newly discovered group termination of the amino acid sequence of isms named by Woese and Fox (1) to of archaebacteria both lacked nuclear insulin in the 1950s (5). Protein bio- distinguish the group from eubacteria]. In membranes. Eukaryotes seemed not de- chemists began to develop phylogenetic describing the phylogenetic relationships, rived from either bacteria or arch- relatedness maps, phylogenetic trees, based on amino acid sequences derived the results also charted the first scientific aebacteria; all three kinds of organisms from various organisms, mainly animals. view of deep evolutionary history. Both seemed to represent aboriginal lines Russell Doolittle sketched out vertebrate these fundamental aspects of biology, the of descent. evolution using blood-clotting fibrinopep- phylogenetic structure of life and the In this retrospective, we view the 1977 tides in the work by Doolittle and Feng course of early evolution, previously were paper by Woese and Fox (1) from three (6); the work by Fitch and Margoliash (7) standpoints. First, we discuss the specific only realms of speculation. used the mitochondrial protein cyto- However, the methods and data used in accomplishments of this landmark paper chrome C to relate animals and some the work by Woese and Fox (1) were and how the program of research initiated fungi. However, not all organisms possess unfamiliar to most biologists, even mo- and led by Woese from the late 1960s to cytochrome C, and for that reason alone, lecular biologists. Traditional biologists, the present day has spawned a revolution fi its amino acid sequence could not be used students of plants and animals, paid little in microbiology and other elds contin- to infer the patterns of relationships attention, because the results had little gent on microbiology, including ecology among all of life. bearing on their interests. Because of and the health sciences. Second, we dis- Carl Woese came to the study of evo- a joint press release by the National cuss the place of that paper in the history lution from a background in biophysics and Aeronautics and Space Administration of evolutionary biology, where its un- and the National Science Foundation that precedented use of molecular sequences ’ fi supported Woese s research, the paper associated with rRNA provided the rst Author contributions: N.R.P., J.S., and N.G. wrote the paper. was heralded on the front page of The New window into the deep timeline of life, one The authors declare no conflict of interest. York Times for discovery of “a third form independent of theoretical prejudices that This article is a PNAS Direct Submission. of life” (2). However, the few biologists had flawed earlier efforts to classify life. See Classic Article “Phylogenetic structure of the prokary- who noticed sometimes reacted negatively, Finally, we describe how the under- otic domain: The primary kingdoms” on page 5088 in issue and articles denouncing the claims were standings sparked by the paper are bring- 11 of volume 74. published. Subsequent developments ing a new face to the study of evolution by See Classic Profile on page 1019. showed that the methods and conclusions compelling biologists to address founda- 1To whom correspondence should be addressed. E-mail: of the paper were sound. tional issues related to the very concepts of [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1109716109 PNAS | January 24, 2012 | vol. 109 | no. 4 | 1011–1018 an interest in the genetic code and its RNases, and the sequences of the resulting origins. During the early 1960s, the nature oligonucleotides were determined by di- of protein synthesis and the makeup of the gestion with other nucleases. Next, frag- genetic code were just being worked ments of incomplete digestion of the RNA out (8). Woese was a contributor to early were isolated and digested completely, thought on the genetic code and had and the digestion products were analyzed; conducted experimental studies to try to eventually, the sequence could be inferred understand the chemical basis of the ca- from the oligonucleotide contents of nonical assignments of different amino overlapping fragments. Mitchell Sogin, acids to particular codons (the DNA or then a graduate student with Woese, RNA base triplets that specify the amino learned the techniques from David H. L. acid sequence of a protein during protein Bishop, a postdoctoral student from synthesis) (9). His 1967 book The Genetic Fred Sanger’s laboratory who was then Code: The Molecular Basis for Genetic working in the Sol Spiegelman laboratory Expression focused prescient attention on at the University of Illinois. Sogin set up the RNA elements of the protein synthe- the necessary facility for Woese’s group. sizing machinery (10). Woese, along with Woese and his students determined sev- Francis Crick (11) and Leslie Orgel (12) eral bacterial 5S rRNA sequences. They after him, are considered founding cham- showed that the rRNA sequences could be pions of the idea that nucleic acids played used as phylogenetic markers for bacteria more than template roles in the origin of (15). They also showed that evolutionary biological systems, thus giving rise to the variation in sequences could be used to notion of a hypothetical prebiotic RNA determine how the RNAs fold into sec- world in which nucleic acids served as both ondary structure (so-called phylogenetic catalytic entities and genetic templates comparative RNA structure analysis) (16). (13). Woese was concerned that the However, it soon became clear that 5S Fig. 1. Ribonuclease T1 oligonucleotide finger- emerging paradigm for the mechanism of rRNA, at only 120 nt in length, was too print. As outlined in the text, data reported in the protein synthesis was too static and had small in size and hence, information con- paper by Woese and Fox (1) in 1977 consisted of no evolutionary dimension. As early as tent to provide for accurate phylogenetic catalogs of oligonucleotide sequences derived 1969, as articulated in a letter to Francis assessments. from RNase T1 digestion of small subunit (SSU) Crick, he understood that the only way to The SSU rRNA, at 1,500–2,000 nt, was rRNAs. The first step of the analysis involved res- reveal the essence of the process was to information-rich, but because of its rela- olution of RNase T1 digests of 32P-labeled rRNA study its conservation and variation in tively large size, it was practically impos- by 2D electrophoresis and locating labeled oligo- different organisms—its evolution—in sible to determine the entire sequence nucleotides on the 80 × 100-cm sheet of electro- a phylogenetic framework.
Load more

Recommended publications
  • (1928-2012), Who Revol
    15/15/22 Liberal Arts and Sciences Microbiology Carl Woese Papers, 1911-2013 Biographical Note Carl Woese (1928-2012), who revolutionized the science of microbiology, has been called “the Darwin of the 20th century.” Darwin’s theory of evolution dealt with multicellular organisms; Woese brought the single-celled bacteria into the evolutionary fold. The Syracuse-born Woese began his early career as a newly minted Yale Ph.D. studying viruses but he soon joined in the global effort to crack the genetic code. His 1967 book The Genetic Code: The Molecular Basis for Genetic Expression became a standard in the field. Woese hoped to discover the evolutionary relationships of microorganisms, and he believed that an RNA molecule located within the ribosome–the cell’s protein factory–offered him a way to get at these connections. A few years after becoming a professor of microbiology at the University of Illinois in 1964, Woese launched an ambitious sequencing program that would ultimately catalog partial ribosomal RNA sequences of hundreds of microorganisms. Woese’s work showed that bacteria evolve, and his perfected RNA “fingerprinting” technique provided the first definitive means of classifying bacteria. In 1976, in the course of this painstaking cataloging effort, Woese came across a ribosomal RNA “fingerprint” from a strange methane-producing organism that did not look like the bacterial sequences he knew so well. As it turned out, Woese had discovered a third form of life–a form of life distinct from the bacteria and from the eukaryotes (organisms, like humans, whose cells have nuclei); he christened these creatures “the archaebacteria” only to later rename them “the archaea” to better differentiate them from the bacteria.
    [Show full text]
  • Portrait: Otto Kandler Und Die Moderne Mikrobiologie
    PORTRAIT Otto Kandler und die moderne Mikrobiologie Hans E. Müller, Braunschweig Regime hielt ihn davon ab, die für Abiturienten damals fast obligaten Off,rzierskurse zu absolvieren. So kam er zu Kriegsende als Unteroffizier in amerikanische Gefangen- schaft und wurde bereits im Juni 1945 wieder entlassen. Studium Nach kurzer Tätigkeit in der väterlichen Gärtnerei schrieb sich Otto Kandler im April 1946 an der Universilät Mün- chen ein und begann ein Snrdium der Biologie und Chemie ftir das höhere Lrhrfach. Um die verlorene Zeit nachzuho- len, wurde damals in Trimestern studiert, und er konnte bereits mit Beginn des vierten Trimesters im Herbst 1947 seine Doktorarbeit beginnen. Die Anregung dazu stammte von dem Virologen und Hygieniker Prof. Gustav Seiffert, der zu dieser Zeit Leiter der Gesundheitsabteilun3 im Bayerischen Innenministerium war. Während gemeinsamer Exkursionen mit der Bayerischen Botanischen Gesellschaft hatte ihm Seiffert von seiner jahrelangen Suctle nach den Urbakterien erzählt, bei der ihm 1936 allerdings Laidlaw und Elford zuvorgekommen waren (52). Die beiden Eng- Einleitung länder hatten damals ebenso wie Seiffert (6L, 62) Abwas- ser filtriert und darin Acholeplasma laidlawii entdeckt. Die naturwissenschaftliche Mikrobiologie ist erst Jahr- Heute wissen wir, daß es zwar nicht die ältesten Lebewe- zehnte nach der medizinischen ein eigenes Fach gewor- sen, wohl aber die primitivsten und kleinsten Saprophyten den, und so hat sie ihre Methoden zunächst von der sind. "Am liebsten hlitte ich gleich mit Arbeiten an diesen medizinischen Mikrobiologie übernommen. Doch längst Organismen begonnen, um Zugang zu Fragen der Evolu- hat sich das Verhältnis umgekehrt. Seit die Molekularbio- tion und Phylogenie zu erhalten", erinnerte sich Otto logie die Forschung dominiert, bekam die medizinische Kandler noch 45 Jahre später (40), denn dieses Thema Mikrobiologie ihre wichtigsten Impulse aus dem wurde zum Leitmotiv in seiner wissenschaftlichen Lauf- naturwissenschaftlichen Fach, und hier war Otto Kandler bahn.
    [Show full text]
  • Classification.Pdf
    Hickman−Roberts−Larson: 4. Classification and Text © The McGraw−Hill Animal Diversity, Third Phylogeny of Animals Companies, 2002 Edition 4 •••••• chapter four Classification and Phylogeny of Animals Order in Diversity Evolution has produced a great diversity of species in the animal kingdom. Zoologists have named more than 1.5 million species of animals, and thousands more are described each year.Some zoologists estimate that species named so far constitute less than 20% of all living animals and less than 1% of all those that have existed. Despite its magnitude, diversity of animals is not without lim- its. There are many conceivable forms that do not exist in nature, as our myths of minotaurs and winged horses show.Animal diversity is not random but has a definite order.Characteristic features of humans and cattle never occur together in a single organism as they do in mythical minotaurs. Nor do the characteristic wings of birds and bodies of horses occur together naturally as they do in the myth- ical horse Pegasus. Humans, cattle, birds, and horses are distinct groups of animals, yet they do share some important features, includ- ing vertebrae and homeothermy,that separate them from even more dissimilar forms such as insects and flatworms. All human cultures classify familiar animals according to pat- terns in animal diversity.These classifications have many purposes. Animals may be classified in some societies according to their useful- ness or destructiveness to human endeavors. Others may group ani- mals according to their roles in mythology.Biologists group animals according to their evolutionary relationships as revealed by ordered patterns in their sharing of homologous features.
    [Show full text]
  • Perspective Default Taxonomy: Ernst Mayr's View of the Microbial World
    Proc. Natl. Acad. Sci. USA Vol. 95, pp. 11043–11046, September 1998 Perspective Default taxonomy: Ernst Mayr’s view of the microbial world (taxonomic domainsyphylogenyyuniversal ancestorybiological classification) Carl R. Woese* Department of Microbiology, University of Illinois at Urbana–Champaign, B103 Chemical and Life Sciences Laboratory, MC-110, 601 South Goodwin Avenue, Urbana, IL 61801 Contributed by Carl R. Woese, July 29, 1998 ABSTRACT This perspective is a response to a taxonomic was never in doubt). These early microbiologists were troubled, proposal by E. Mayr [“Two empires or three?” (1998) Proc. for one, by the fact that “prokaryote” (a term they rarely used) Natl. Acad. Sci. USA 95, 9720–9723]. Mayr has suggested that was defined on the basis of “entirely negative characteris- the now accepted classification of life into three primary tics”—as not possessing certain eukaryotic traits (7). For domains, Archaea, Bacteria, and Eucarya—originally pro- another, the morphological and physiological diversity they posed by myself and others—be abandoned in favor of the encountered among bacteria readily led them intuitively to earlier Prokaryote–Eukaryote classification. Although the consider that the various major bacterial groups “are of matter appears a taxonomic quibble, it is not that simple. At polyphyletic origin” (8). issue here are differing views as to the nature of biological Nevertheless, microbiologists eventually did come around, classification, which are underlain by differing views as to accepting that “prokaryote,” like “eukaryote,” was indeed a what biology is and will be—matters of concern to all biolo- monophyletic taxon. The apparent reason for this remarkable gists. change in the microbiologist’s outlook was that by the 1960s technology had reached the point where it was possible to In his article “Two empires or three?” recently published in this define the prokaryote in positive rather than solely in negative journal (1), Ernst Mayr rejects the three-domain structuring of terms (4).
    [Show full text]
  • A Computer Scientist's Guide to Cell Biology
    A Computer Scientist’s Guide to Cell Biology A Computer Scientist’s Guide to Cell Biology A Travelogue from a Stranger in a Strange Land William W. Cohen Machine Learning Department Carnegie Mellon University William W. Cohen Machine Learning Department Carnegie Mellon University Pittsburgh, PA 15213 USA [email protected] Library of Congress Control Number: 2007921580 ISBN 978-0-387-48275-0 e-ISBN 978-0-387-48278-1 Printed on acid-free paper. © 2007 Springer Science+Business Media, LLC All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. 9 8 7 6 5 4 3 2 1 springer.com To Susan, Charlie, and Joshua. Table of Contents List of Figures ........................................................................... xi Introduction............................................................................. xiii How Cells Work........................................................................
    [Show full text]
  • Perspective Default Taxonomy: Ernst Mayr's View of the Microbial World
    Proc. Natl. Acad. Sci. USA Vol. 95, pp. 11043–11046, September 1998 Perspective Default taxonomy: Ernst Mayr’s view of the microbial world (taxonomic domainsyphylogenyyuniversal ancestorybiological classification) Carl R. Woese* Department of Microbiology, University of Illinois at Urbana–Champaign, B103 Chemical and Life Sciences Laboratory, MC-110, 601 South Goodwin Avenue, Urbana, IL 61801 Contributed by Carl R. Woese, July 29, 1998 ABSTRACT This perspective is a response to a taxonomic was never in doubt). These early microbiologists were troubled, proposal by E. Mayr [“Two empires or three?” (1998) Proc. for one, by the fact that “prokaryote” (a term they rarely used) Natl. Acad. Sci. USA 95, 9720–9723]. Mayr has suggested that was defined on the basis of “entirely negative characteris- the now accepted classification of life into three primary tics”—as not possessing certain eukaryotic traits (7). For domains, Archaea, Bacteria, and Eucarya—originally pro- another, the morphological and physiological diversity they posed by myself and others—be abandoned in favor of the encountered among bacteria readily led them intuitively to earlier Prokaryote–Eukaryote classification. Although the consider that the various major bacterial groups “are of matter appears a taxonomic quibble, it is not that simple. At polyphyletic origin” (8). issue here are differing views as to the nature of biological Nevertheless, microbiologists eventually did come around, classification, which are underlain by differing views as to accepting that “prokaryote,” like “eukaryote,” was indeed a what biology is and will be—matters of concern to all biolo- monophyletic taxon. The apparent reason for this remarkable gists. change in the microbiologist’s outlook was that by the 1960s technology had reached the point where it was possible to In his article “Two empires or three?” recently published in this define the prokaryote in positive rather than solely in negative journal (1), Ernst Mayr rejects the three-domain structuring of terms (4).
    [Show full text]
  • Scientific, Historical, and Conceptual Significance of the First Tree of Life
    PNAS CLASSIC PERSPECTIVE Phylogeny and beyond: Scientific, historical, and conceptual significance of the first tree of life Norman R. Pacea,1, Jan Sappb, and Nigel Goldenfeldc aDepartment of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, CO 80309; bBiology Department, York University, Toronto, ON, Canada M3J 1P3; and cInstitute for Genomic Biology and Department of Physics, University of Illinois, Urbana, IL 61801 Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved December 20, 2011 (received for review November 29, 2011) In 1977, Carl Woese and George Fox published a brief paper in PNAS that established, for the first time, that the overall phylogenetic structure of the living world is tripartite. We describe the way in which this monumental discovery was made, its context within the historical development of evolutionary thought, and how it has impacted our understanding of the emergence of life and the characterization of the evolutionary process in its most general form. fundamental breakthrough in Several aspects of the paper by Woese species and organism and bringing to the biological science occurred in and Fox (1) sparked skepticism. One fore the deep limitations of earlier ac- A 1977, and most biologists did was the arcane nature of the molecular counts of the evolutionary process. not notice. The paper by Woese data, which few could appreciate. The re- and Fox (1) in 1977 was 2.5 pages in length liance on a single gene to trace major Lead Up to the Paper and contained a single table of numbers trends in evolution was an equally alien The 1977 paper by Woese and Fox (1) was that compared sequence snippets derived concept.
    [Show full text]
  • The Structure of Microbial Evolutionary Theory
    Available online at www.sciencedirect.com Studies in History and Philosophy of Biological and Biomedical Sciences Stud. Hist. Phil. Biol. & Biomed. Sci. 38 (2007) 780–795 www.elsevier.com/locate/shpsc The structure of microbial evolutionary theory J. Sapp Department of Biology, Faculty of Science and Engineering, York University, 4700 Keele St, Toronto, Ontario M3J 1P3 Canada Abstract The study of microbial phylogeny and evolution has emerged as an interdisciplinary synthesis, divergent in both methods and con- cepts from the classical evolutionary biology. The deployment of macromolecular sequencing in microbial classification has provided a deep evolutionary taxonomy hitherto deemed impossible. Microbial phylogenetics has greatly transformed the landscape of evolutionary biology, not only in revitalizing the field in the pursuit of life’s history over billions of years, but also in transcending the structure of thought that has shaped evolutionary theory since the time of Darwin. A trio of primary phylogenetic lineages, along with the recogni- tion of symbiosis and lateral gene transfer as fundamental processes of evolutionary innovation, are core principles of microbial evolu- tionary biology today. Their scope and significance remain contentious among evolutionists. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Microbial evolution; Microbial phylogeny; Procaryote; Superkingdoms; Symbiosis; Lateral gene transfer When citing this paper, please use the full journal title Studies in History and Philosophy of Biological and Biomedical Sciences 1. Introduction microbes, their relationships to one another and to other organisms, than they did in the time of Pasteur and Koch. The evolutionary synthesis of the first half of the twen- The emergence, of microbial phylogenetics, based on tieth century crafted a sterile conception of evolution: one macromolecular sequencing, has brought great change to without microorganisms.
    [Show full text]