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Journal of Bacteriology, April 2009, p. 2006-2007, Vol. 191, No. 7
0021-9193/09/$08.00+0 doi:10.1128/JB.01296-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
| DIALOG |
Rebuttal: the Modern Concept of the Procaryote 
Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309-0347
At issue here is the scientific validity of the procaryote concept. W. B. Whitman (3) embraces the term and concept of procaryote that were introduced into microbiology by R. Y. Stanier and his colleagues in the early 1960s. The procaryote concept was a specific hypothesis that postulated that (i) there are fundamentally two kinds of cells, procaryotes and eucaryotes, and (ii) procaryotes are defined by their particular cellular organization, one distinct from that of eucaryotes. W. B. Whitman believes that the Stanier definition needs to be modernized to be more specific in the definition of the "procaryote." His "modern concept" of the procaryote includes two phylogenetic groups of organisms, bacteria and archaea, because both lack the eucaryotic cell structure.
The procaryote-eucaryote hypothesis, with no specific definition of the procaryote and no experimental test, was incorporated into the common wisdom of biology. When the experimental test came, with the discovery of archaea in 1977, the validity of the procaryote taxon was disproved. "Procaryotes" were determined molecularly to consist of two kinds of organisms, the traditional bacteria (taxon Bacteria) and archaea (formally, Archaea), which are not specifically related. Moreover, it was discovered that bacteria and archaea do not share the same cellular organization when looked at more carefully in the light of the molecular evidence. Eucaryotes (domain Eucarya) constitute a monophyletic group, but there is no phylogenetic group that corresponds to procaryotes. Additionally, the molecular data show that the eucaryotic nuclear line of descent is derived from neither bacteria nor archaea but from something more primitive than either.
W. B. Whitman's rationale for the grouping of noneucaryotes, his defense of the procaryote, is not convincing. Indeed, he concludes that "... examination of the distinct and shared characters between the Archaea and Bacteria provides compelling evidence for two domains." That is true. Then why try to conflate them conceptually?
W. B. Whitman improperly uses the rRNA tree of life to illustrate his modern concept of the procaryote. He shows an unrooted three-domain tree and brackets Bacteria and Archaea to illustrate his concept of the procaryote. But he omits the root of the tree, which separates the bacterial line of descent from that which led to archaea and eucaryotes. The root of the tree fundamentally separates Bacteria from Archaea. There is no natural grouping that corresponds to the term procaryote.
W. B. Whitman admits this: "The procaryotic classification could also be criticized because it is paraphyletic, but this objection is not substantive if the identification of monophyletic groups is not a major goal of the classification."
But the identification of monophyletic groups is a major goal of scientific classification, and the results should capture the patterns of evolution. With his admission that his procaryote is not a phylogenetically coherent group, W. B. Whitman contradicts Charles Darwin ("Our classifications will come to be, as far as they can be so made, genealogies." [1]) and even Stanier, who, with colleagues M. Doudoroff and E. A. Adelberg, espoused "... grouping living organisms in the manner which expresses best the degree of their evolutionary relatedness" (2).
A key point here, one generally missed in debates about the procaryote concept, is that as scientists we do not have the luxury of making a classification based on arbitrary criteria. As scientists, we must observe nature and classify accordingly. A conceptually sound classification scheme should smoothly converge as data accrue, because the data do not, and cannot, undermine the scientific principle that underlies a valid classification scheme. One hallmark of a capricious classification scheme is that it will be "high maintenance," sometimes requiring radical readjustment as the underlying assumptions are contradicted by data. Fortunately, in biology there is one, and only one, relationship that has been uniquely defined over the last four billion years—the evolutionary relationship between organisms. The procaryote concept is discredited by the evolutionary data.
W. B. Whitman's proposal of a modern concept of the procaryote has all the hallmarks of a high-maintenance classification scheme, and his essay clearly indicates the way in which the procaryote concept needs to be continually reworked to keep pace with scientific discovery. Yet, at the same time the concept fails to make testable scientific predictions.
My goal in this debate series has been to expose the problems with the procaryote concept and why it needs to be relegated to the history of biology. W. B. Whitman does not explain what is the goal of his defense of the procaryote concept. Why promote bad phylogeny and the concomitantly flawed grouping? Why try to resurrect a disproved hypothesis? How can such a muddled concept as that of the procaryote, with no specific definition, contribute to progress toward a better understanding of biology? Our scientific understanding of the deepest genealogy of life has advanced greatly over the past 3 decades of molecular discovery. The concept of the procaryote, traditional or "modern," denies that progress.
W. B. Whitman's "modern procaryote" concept needs to be rejected because, rather than clarifying the issue, it confuses it further. The original procaryote concept at least was a testable scientific hypothesis, even though upon testing it proved false. W. B. Whitman's modern procaryote concept seems to me not only false because it is based upon the original disproved assertion but also because it is mushy to the point of being untestable. The procaryote concept is a high-maintenance concept with no useful predictive value.
I thank Carl Woese and Nigel Goldenfeld for many comments and contributions to the text.
* Mailing address: Department of Molecular, Cellular, and Developmental Biology, Campus Box 0347, University of Colorado, Boulder, CO 80309-0347. Phone: (303) 735-1864. Fax: (303) 492-7744. E-mail: nrpace{at}colorado.edu
Published ahead of print on 23 January 2009.
- Darwin, C. 1882. On the origin of species by natural selection, or the preservation of favored races in the struggle for life, 6th ed., p.427. D. Appleton & Co., New York, NY.
- Stanier, R. Y., M. Doudoroff, and E. A. Adelberg. 1963. The microbial world, 2nd ed. Prentice-Hall, Inc., Englewood Cliffs, NJ.
- Whitman, W. B. 2009. The modern concept of the procaryote. J. Bacteriol. 191:2000-2005.
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Journal of Bacteriology, April 2009, p. 2006-2007, Vol. 191, No. 7
0021-9193/09/$08.00+0 doi:10.1128/JB.01296-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
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