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microbiology vol36|may09 quarterly magazine of the society today for general

microbiology vol 36 | may 09

darwin 200 darwin and the origin of infection the phylogenomic species concept retire the prokaryote a microbial cockatrice a glimpse of micro-evolution virus evolution xperimental results rarely upset the common wisdom of a scientific discipline, but that Norman R. Pace happened to biology late in the 20th century. The common wisdom in deep evolution and believes that the term how we classify organisms was rendered sorely It’s time in need of modernization. And that modern- Eization is happening too slowly. ‘prokaryote’ is an The anachronism here is the notion of ‘prokaryote’ and the model of biological organization and evolution that it elicits. anachronism in modern This model, which I term the ‘prokaryote–eukaryote’ model, to retire posits that fundamentally there are two kinds of organisms, prokaryotes and eukaryotes, defined by the presence or biology. Here he explains absence of a nucleus (more properly nuclear membrane). Additionally, the model proposes that prokaryotes gave rise to eukaryotes, as shown in the figure overleaf. the why and seeks the The problem, however, is that the prokaryote concept has been undermined critically by sequence-based phylogenetic help of microbiologists results. Indeed, the notion of prokaryote was scientifically illogical from the beginning because the definition, an ‘organism without a nucleus’, is a negative definition. No prokaryote in stopping its use. one can tell you what a prokaryote is, interchangeable in the textbooks with they can only tell you what it is not. ‘prokaryote’. It is curious that the Yet, institutional biology embraced nomenclature of ‘monera’ never caught- the notion of prokaryote and it came on among earlier microbiologists, to dominate textbooks, journals and whereas ‘prokaryote’ was immediately discourse in matters of deep evolution. incorporated into the lexicon. But in But the hypothesis of the prokaryote fact, prokaryote was never much more was never tested. than a name-change from monera, a 19th century notion based on far Where it came from – more limited knowledge than is now the very short history of available. prokaryote It is important to understand that The disproof of prokaryote the concept of prokaryote is not The idea of prokaryote was disproved based on scientific results. Rather, it in 1977, with Carl Woese’s discovery is based on historical conjecture. To of archaea and the first articulation of simplify the history considerably, I a rudimentary molecular phylogenetic think that prokaryote had its origins tree that related the most diverse in evolutionary models of the late forms of life. Woese saw through 1800s, with ‘monera’ at the origin of comparisons of ribosomal RNA a tree of complex eukaryotes. Monera (rRNA) sequences that life’s diversity persists today at the base of the five- is composed not of two deeply related kingdom classification scheme, which groups, prokaryote and eukaryote, but was introduced in the 1960s and is rather three such groups. These three popular in current textbooks. Also in phylogenetic ‘domains’ came to be the 1960s, the name ‘monera’ became called Bacteria, Eukarya (eukaryotes, which indeed proved monophyletic) and Archaea. Woese originally named the latter group Archaebacteria, but ᭣ ‘Prokaryotes’ heading into the sunset. this was changed to Archaea when it Medical R.F.Com / Science Photo Library (bacteria); Photos.com/Jupiter Images became clear they are fundamentally (sunset) distinct from Bacteria.

84 microbiology today may 09 microbiology today may 09 85 (a) Prokaryote–eukaryote model (b) Three-domain model

Bacteria

Origin Origin

Prokaryotes Eukaryotes Eukarya

᭡ Prokaryote–eukaryote (a) versus three-domain (b) models for biological organization and the course of deep evolution. The wedges indicate radiations within the respective groups.

Archaea

The three-domain model of relationships and evolution the nuclear membrane. At the last resort, the proponents What to do about it and how modernization. This is because their to be sure, but it also provides a stands in stark contrast to the prokaryote–eukaryote model, of prokaryote insist, ‘You have to call them something!’ But microbiologists are critical organisms span the three domains, solid foundation for progress toward as shown in the figure above. The three-domain pattern that’s the problem: there isn’t any ‘them’. The molecular Institutional biology is now heavily and the phylogenetic perspective is answering those questions. shows that eukaryotes constitute a phylogenetically coherent phylogenetic results, bolstered by decades of biochemical invested in the prokaryote concept. referentially necessary and an obvious group, but there is no specific group to label ‘prokaryote’. corroboration, show that there is no natural grouping that The language permeates our literature utility. Modern treatment of issues Norman R. Pace Both archaea and bacteria would qualify through their would correspond to prokaryote. and thereby distorts understanding of in classification and evolution by Department of MCD Biology, lack of a nuclear membrane, but these two groups are Proponents of the concept of the prokaryote sometimes foundational issues. One hurdle that microbiological journals and textbooks University of Colorado, Boulder, not specific relatives. Indeed, archaea are more closely argue that the prokaryote terminology is a convenient faces efforts to modernize this matter eventually will lead to upgraded CO 80309-0347 (e nrpace@ related to eukaryotes than archaea are to bacteria. This classification and that historical usage justifies contin- is that most students, biologists and general texts. One catalytic step that colorado.edu) relationship is supported not only by molecular phylogeny, ued usage. But these rationalizations are scientifically authors of general textbooks don’t any microbiologist can contribute, but also by many properties of archaeal and eukaryotic inappropriate. A critical point here, one usually missed think very much about microbes. however, is simply to stop using the cells compared to bacterial cells. by proponents of the prokaryote concept, is that scientific Their world is generally that of large term ‘prokaryote’. This may be hard to Further reading Additionally, the phylogenetic model shows no specific classification is not a convenience. As scientists we must organisms of limited diversity. They, do because of long conditioning, but Pace, N.R. (1997). A molecular view group of organisms that preceded the eukaryotes. The observe nature and classify accordingly, so as to promote unlike microbiologists, are not faced it is an important step for educators of microbial diversity and the biosphere. textbook and common wisdom that eukaryotic cells arose scientific understanding. As Darwin insisted, ‘Our classifi- with trying to make sense of a vast particularly. Science 276, 734–740. late in the history of Earth by fusion of two prokaryotes is cations will come to be, as far as they can be so made, genealogies’. diversity of life with comparatively How can teachers broach this issue Sapp, J. (2005). The prokaryote– incorrect. Mitochondria and chloroplasts were derived from ‘Prokaryote’ doesn’t fit the observed genealogy. It needs to little observable variation without in the face of the currently pervasive eukaryote dichotomy: meanings and symbiotic bacteria, but the nucleus is far more ancient. The be retired from the language of biology. It has become a resort to biochemistry and gene reference to prokaryotes in journals mythology. Microbiol Mol Biol Rev 69, history of the nucleus is seen in the molecular phylogenetic distraction. sequences. The three-domain phylo- and textbooks? One way to do so is to 292–305. tree as the eukaryal line of descent. The tree shows that the genetic model is beginning to appear use the discordance between recently Woese, C.R. (1994). There must be a nuclear line is as old as the archaeal line and was derived Why it matters in textbooks, but usually as just emerging data and the textbooks as a prokaryote somewhere: microbiology’s from neither archaea nor bacteria. The molecular results The legitimacy of prokaryote is more than an issue in another method of classification, prime example of how science, biology search for itself. Microbiol Mol Biol Rev say nothing at all about whether or not the earliest terminology. It is also a matter of proper understanding alongside the five-kingdom scheme. in this case, is an ongoing, living 58, 1–9. eukaryotes possessed nuclear membranes. In the light of of important biological concepts. Any scientific field rests The evolutionary implications of the process, evolving in response to new Woese, C.R. & Goldenfeld, N. the sequence comparisons, the presence or absence of the essentially on two conceptual foundations. One foundation three-domain pattern of evolution are experimental data. Dealing with the (2009). How the microbial world nuclear membrane or other morphological trait is irrelevant requires understanding of the order, the organization of seldom broached, and the language prokaryote issue is an opportunity saved evolution from the Scylla of for classification or for deduction of the paths of deep the subjects of study. The other conceptual foundation is of prokaryote perseveres. What to do to demonstrate the testing of specific molecular biology and the Charybdis evolution. how the subjects of study change. Foundational issues for about it? hypotheses with experimental data, of the Modern Synthesis. Microbiol progress in biology, therefore, are proper perceptions of The retirement of prokaryote from with results important for biology. Mol Biol Rev 73, 14–21. Some would argue phylogenetic groups and relationships and, consequently, the lexicon of biology will be slow Phylogenetic trees, maps of evo- Some authors defend prokaryote as a useful classification. the path of evolution. because it is now so deeply entrenched. lutionary relationships, are straight- They argue, for instance, that bacteria and archaea are united The prokaryote–eukaryote notion fails in both these Consequently, that retirement process forward metaphors for the course of by their very small size or their use of coupled transcription regards. In contrast, the three-domain pattern of life’s organi- needs to be catalysed. Microbiologists evolution and are not hard for students and translation. These arguments are not meaningful; rather, zation and large-scale path of evolution is solidly grounded are in the best position to understand to understand in essence. The three- they are just other twists on the presence or absence of on scientific observations. the issues and to participate in domain concept poses many questions,

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