Two empires or three?

In the last 100 years, several spectacular discoveries were made in the world of biodiversity, discoveries such as the Okapi in the Congo forest, the only living relative of the giraffes, or Latimeria in the Indian Ocean, a living coelacanth fish, believed to have been extinct for 60 million years. But these were merely small white spots on the world map of biodiversity. By contrast, Carl Woese’s discovery of the archaebacteria was like the discovery of a new continent. Where should one place this new group of microorganisms? From antiquity until the twentieth century, the traditional division of the living world was into animals and plants. Even today, biology is taught in zoology and botany departments in many colleges and universities, particularly abroad. Botany, for a long time, was defined as including anything living that is not an animal. As a result, the study of fungi and bacteria was assigned to botany departments. Indeed, in the nineteenth century, some of the leading bacterial taxonomists had their professorships in botany departments. The subdivisions within animals and plants were equally unbalanced. After 1859, the study of phylogeny produced great advances in our understanding of the relationship of animals. The recognition by Grobben (1) that ‘‘above’’ the coelenterates there are two major groupings of animals, the Protostomia and the Deuterostomia, was a great leap forward. The most important recent development, of course, was the use of molecular methods in the field of classification. Although usually confirming the results of morphological analysis, molecular methods are all-important in all cases of controversy and/or uncertainty. It is now only a question of time until the true relationship of all phyla and classes of animals is firmly established. Although foreshadowed by suggestions made by earlier authors, by far the most important advance made in our understanding of the living world as a whole was the realization by Chatton (1937) (2) that there are two major groups of organisms, the prokaryotes (bacteria) and the eukaryotes (organisms with nucleated cells). This classification was confirmed and made more widely known by Stanier and van Niel (3), and it was universally accepted by biologists until recently. As far as the eukaryotes are concerned, it was soon realized that the fungi are not plants; in fact, molecular studies showed that they are actually more closely related to animals. All single-celled eukaryotes were at first placed into the phylum Protista. Although recent studies, particularly molecular analyses, have shown that the Protista are a very heterogeneous assemblage, consisting of single-celled algae (formerly plants), protozoans (formerly animals), water molds (formerly fungi), and members of many other groups, it is still convenient to speak of unicellular eukaryotes in the vernacular as protists. The number and kind of higher taxa of eukaryotes one should recognize for the various types of protists, in addition to the kingdoms of plants, fungi, and animals, are still under discussion. The classification of the prokaryotes was chaotic until very recently. Woese (4) considerably clarified by molecular analysis the relationship of the various kinds of bacteria to each other and determined what kind of classification one should adopt. By far his most important discovery was that the prokaryotes actually consist of two major groups: (i) the traditional bacteria, at first best known from the study of human diseases, and (ii) a previously unrecognized group of bacteria, named by Woese (5) archaebacteria. This group is not only quite different from the eubacteria, as Woese renamed the traditional bacteria, but also of special interest for two reasons. The first reason is that they contain all sorts of highly specialized organisms that can live in very unusual environments, which at first sight would seem totally unsuited for life, such as hot springs, sulfur springs, brines, etc. However, in recent years it has been found that archaebacteria are also common in many normal environments, such as sea water, rice fields, and marshes (6). Even more interesting was the discovery that the archaebacteria share many important genes with the eukaryotes; indeed, further studies proved that the eukaryotes had an archaebacterial root. Woese baptized the newly discovered organisms archaebacteria, thinking they would have been the first organisms on the newly habitable earth because of their ability to live in an anoxic atmosphere and in hot springs, sulfur springs (thermoacidophiles), brines (halophiles), and other unusual habitats, presumably common on the new earth. However, when it later appeared probable that they were not the most ancient bacteria and might have a common stem with the eubacteria, Osawa and Hori (7) suggested replacing the misleading name archaebacteria by metabacteria. Neither Woese (8) nor other microbiologists accepted this change of name. Instead Woese renamed them Archaea, retaining the inappropriate component—archae—and discarding the informative component— bacteria, which revealed their prokaryote nature. Woese’s discoveries and interpretations were widely acclaimed and accepted, with one exception. Woese was so impressed by the distinctness of this new group of bacteria that he proposed to give the same categorical rank to the archaebacteria as to the totality of all eukaryotes. Instead of recognizing the two traditional taxa of organisms, the prokaryotes and the eukaryotes, he proposed to recognize three domains, the eubacteria, the archaebacteria, and the eukaryotes (8). It was this proposal that created considerable opposition, particularly outside microbiology. Woese in his early work apparently based his decision on two assumptions, that the eubacteria and archaebacteria had independently arisen from the progenote, his hypothetical universal ancestor of life, and that ‘‘on the molecular level [the archaebacteria] resemble other prokaryotes, the eubacteria, no more (probably less) than they do the eukaryotes’’ (8). Both assumptions were soon refuted, and Woese now bases his three-domain arrangement on