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). Yet, on closer examination this conceptual reversal the living world—Archaea, Bacteria, and Eucarya—that has seems more a matter of a new-found faith than of any emerged from molecular studies over the past two decades (2). new-found facts (3): in defining the prokaryote in the new He would return to the older Prokaryote–Eukaryote classifi- cytological and molecular terms, there were “remarkably few cation, which shaped biology’s overview of life on this planet comparative studies, [which means that] the application of the for the last half century. I have argued previously that, from the newer [techniques] for taxonomic purposes entails generali- outset, the prokaryote–eukaryote dichotomy was an idea zation from limited cases” (9). In other words, nobody at the never properly tested (3). And I believe the complacency that time felt it necessary to ask whether certain properties of this simplistic formulation generated adversely affected the Escherichia coli and occasionally a few other bacteria were development of biology, for it served among other things to actually properties of prokaryotes in general. The monophy- mask the fact that the basis for a true science of microbiology, letic nature of prokaryotes was simply taken for granted! Why “the concept of a bacterium” (4), was never developed. To would microbiologists do this; why would they trade their return to the prokaryote–eukaryote dogma (with its lingering previous scientific skepticism for an untested belief? The false connotations) would have a similarly negative effect now, reason, I think, is that a monophyletic prokaryote appeared to once again on microbiology, but this time too on the study of relieve microbiologists of the necessity of determining phylo- evolution—both of these fields currently in states of revolu- genetic relationships in order to develop a “concept of a tionary development. bacterium” (3, 4). I am not inclined to reply to Dr. Mayr’s article in detail or For at least the first half of this century determining in kind, although some of the former is required. Dr. Mayr and microbial phylogenetic relationships had proven impossible, I see things from very different perspectives, and it is this and their repeated failures to do so seem to have brought some difference in perspective, not some local taxonomic dispute, (perhaps most) microbiologists to believe that these relation- that needs to be aired. Therefore, I will respond to what Dr. ships were inherently indeterminable, at least at the higher Mayr’s article really is—i.e., a pronouncement concerning the taxonomic levels (6, 10, 11). As a consequence, a default future direction biology should take. position was taken, in which the prokaryotes were simply assumed to be specifically related to one another (4). From The History of the Eukaryote–Prokaryote Dichotomy this, microbiologists of the 1960s then argued that prokaryotes could be defined biologically—that the much needed concept The idea that the living world is divided in the first instance of a bacterium could be developed—simply by cataloging the into two very different types of organisms, prokaryotes and differences between prokaryotes and eukaryotes (4). Of eukaryotes, is generally attributed to Chatton in the 1930s (4, course this did not work, and no one at the time seemed to have 5), but the notion that bacteria (schizomycetes) are somehow appreciated that it could not, which left microbiology and the unique, are the “first and simplest division of living beings,” rest of biology saddled with the false notion that all pro- goes back to the great microbiologist Ferdinand Cohn in the karyotes are of a kind, are specifically related (3). last century (6). Microbiologists of the early twentieth century, however, were loath to accept the principal implication of a Lessons from Genes prokaryote–eukaryote dichotomy—i.e., that all prokaryotes are of a kind (although the monophyletic nature of eukaryotes Technology ultimately came to the rescue, and through the use of ribosomal RNA (rRNA) sequence comparisons it proved © 1998 by The National Academy of Sciences 0027-8424y98y9511043-4$2.00y0 PNAS is available online at www.pnas.org. *e-mail: [email protected]. 11043 11044 Perspective: Woese Proc. Natl. Acad. Sci. USA 95 (1998) possible to determine microbial phylogenetic relationships. At exist on Earth. Now is definitely not a time to alter our the molecular level both the higher and lower prokaryotic taxa classification of organisms so as to suggest that biology’s readily revealed themselves, as did their relationships to one primary focus be on animals and plants and that all bacteria are another and to the eukaryotes (2, 12–15). The resulting of a kind (1). The primary interest today is in cells and universal phylogeny unexpectedly showed that the taxon “pro- molecules, and our study of animals and plants necessarily karyote,” which all biologists (including myself) had hereto- operates in the first instance from this platform. Biology, like fore assumed to be monolithic, in reality comprises two physics before it, has moved to a level where the objects of fundamentally distinct groups of organisms, each no more like interest and their interactions often cannot be perceived the other than they are like eukaryotes (12, 13). Thus, there are through direct observation. And, as in the case of physics, actually three, not two, primary phylogenetic groupings of biology’s “subatomic” (subcellular) level is rich in information, organisms on this planet (2, 12). Moreover, a phylogenetic tree rich in understanding, and rich in beauty. It is at the level of based upon the molecular data shows that the newly recog- molecules that biologists are able to expand their perspective nized one, the Archaea, is, if anything, more closely related to to genuinely encounter the microbial world, the full extent of eukaryotes than to the familiar bacteria (2, 14, 15). Here then which we have still to experience, a world whose metabolic and was biology’s first glimpse of the full evolutionary landscape. phylogenetic diversity completely dwarfs that seen in the Within the framework of a universal phylogenetic tree the animal and plant kingdoms combined. But more important (to study of evolution could now move beyond the confines of the me) is that biology’s incursions into molecules and genomes plant and animal kingdoms and into the enormous realm of have transformed an otherwise rather stale and isolated microorganisms. discipline of evolutionary study into one of the most vibrant, This universal tree, this beautiful and compelling image, has central, and important facets of our science. seen some rough weather of late, not because of Dr. Mayr, but because of the complexity introduced into the picture by the On the Nature of a Biological Classification large amounts of additional sequence data now available, data that reveal the extent to which lateral gene transfer has shaped The nature of biological classification figures heavily in Dr. the evolutionary course over the long haul. As a result, Mayr’s argument, and so must be addressed. In his view the phylogenetic trees based upon protein genes tend not to show present issue can and should be defined and settled in terms deep phylogenetic branchings consistent with the rRNA tree. of established classificatory formalisms. If there were ever an But neither do the branchings in these dissonant trees tend to issue in biological classification that cannot be settled by agree with one another. pedantry, it is this one. Never before has there been a less This state of seeming confusion has given rise to skepticism: subjective highest taxonomic level than that defined by the as to the validity of the rRNA-based phylogenies (16); as to universal phylogenetic tree. To Mayr, the issue is one of whether the deep evolutionary record might have been erased, whether we should define two or three domains and what the and therefore we will never know the nature of the universal classificatory precedents or rules for deciding this are.