How to teach the new understanding of higher-level taxonomy By Laura K. Baumgartner and Norman R. Pace What's in a name? Even the nomenclature for different he ability to sequence genes has vastly altered our un- kinds of organisms can be complicated derstanding of higher-level relationships among or- by the current change in understand- ganisms such as those found at the kingdom level. It is ing. When science textbooks rely on monera and prokaryotes, or even the important for biology teachers to incorporate these new more dated protozoans, what other Tviews and not retain outdated concepts still present in some text- terms can be used? To describe micro- books. This article provides an overview of our new understand- scopic organisms, we suggest microbe, ing of higher-level taxonomy, and suggestions for the utilization which includes microscopic eukaryotes of current taxonomy in classroom instruction. (e.g., amoebae) as well as bacteria and The advent of gene sequencing and other discoveries in biol- archaea. What should be used to de- note anything that is not a eukaryote? ogy over the past three decades has fundamentally changed our We suggest actually using bacteria view of the course of evolution and how organisms are related. and archaea, which allows students Evolutionary distances as measured by DNA sequencing can to adjust to the often-unfamiliar terms be used to create phylogenetic trees or maps of relatedness and before they may encounter them at evolution. Although our understanding of these trees is new and the college level. occasionally contentious, general agreement has emerged from an evaluation of them. These new views dramatically alter our understanding of early evolution and of organismic relationships at the level of the kingdom. 46 The Science Teacher F I G U R E 1 A The three-domain molecular tree of life. Homo (human) represents all animals, Zea (maize) represents all plants, and Coprinus represents all fungi. mitochondrion tomyces Rhodocyclu Planc Esch p Flavobacterium em erichia Methanobacterium t chloro cter SynechococcusDesulfovibrio Archaea s us Thermococcu p Flexiba las t Agrobacterium ChlamydiaGloeobacte marine low Haloferax Me Archaeoglobus Chlorobium t r hanothermu Thermoplasma s Methanococc Methanospirillum Leptonema Methanopyru s marine Gp. 1 low temp Clostridium Gp. 1 s Gp. 2 lowl owtemp temp pSL 12 Bacillus pSL 22 Gp. 3 low temp Heliobacterium Arthrobacter PyrodictiumSulfolobu pOPS19 s ThermofilumThermoproteus Root pSL 50 Thermus pOPS66 pJP 78 Chloroflexus Thermotoga pJP 27 Bacteria Aquifex EM17 Coprinus Ho m o Zea Cryptomonas Eukarya Achlya Costaria ium Porphyra Giardia Babesia Paramec Phys Trichomonas Dictyostelium arum Euglen Trypanosoma Encephalitozoon Entamoeba Naegleria Vairimorpha a October 2007 47 Darwin recommended that biological taxonomy F I G U R E 1 B be based on evolutionary relationships. Taxonomy in many textbooks is based on the “five kingdoms of life,” The three-domain molecular tree of life. typically including Animalia, Plantae, Fungi, Protista, and Monera as proposed by Whittaker in 1969. The Cartoons of the two models of evolution. The triangles indicate five kingdoms are often combined with the concept divergences of genetic lines (e.g., species) within the groups of prokaryote (cells with no nucleus) versus eukaryote represented by each triangle. (cells with a nucleus). Both of these systems for organiz- ing life have largely been replaced in current scientific Previous model: Eukaryotes evolve from understanding with the concept of the three domains, prokaryotes which divides life into Bacteria, Eukarya, and Archaea. Bacteria In some textbooks, the third domain of Archaea has Prokaryotes Eukaryotes been grafted on to the five kingdom tree to create a six kingdom tree, but neither a five- or six-kingdom system properly portrays the evolutionary relationships. Origin Origin Eukarya What has replaced the familiar five kingdoms? Be- ginning in the 1970s, genetic studies have given us an en- tirely new, experimentally grounded perspective on the Current model: Three domains with a common Archaea interrelationships of organisms, culminating in the tree origin of life based on molecular evidence (Figure 1A, p. 47). We present here a short historyProkaryotes of how theEukaryotes five- Bacteria kingdom model came into popular use, how it has been replaced with the three-domain model (Figure 1B), and how this reappraisal can be used in the classroom. Origin Origin Eukarya A brief history of terms Until the mid–20th century there was little understand- ing of microbes and their relationships, and taxonomies Archaea were based on conjecture (Sapp 2005, 2006; Woese 1994). F I G U R E 2 Author(s) Linnaeus Haeckel Chatton Whittaker Woese, Fox Woese et al. Year 1735 1866 1938 1969 1977 1990 System 2 Kingdoms 3 Kingdoms 2 Empires 5 Kingdoms 3 Urkingdoms 3 Domains Major taxonomic Eubacteria Bacteria unit of Bacteria Classified Not Included within Kingdom Prokaryotes Monera Major Protista taxonomic Archaebacteria Archaea unit of Archaea Major taxonomic unit of Vegetabilia Plantae Plantae Eukaryota Eukaryotes Eukaryotae Eukarya Protista Protista Animalia Fungi Animalia Animalia 48 The Science Teacher Current Taxonomy in Classroom Instruction For example, Linnaeus (1735) organized all living things ally came into common usage. (More details about this into merely two kingdoms: Vegetabilia and Animalia. interesting chapter in the history of science are found in In the 19th century, a widely embraced concept was em- Sapp [2005], available online at www.pubmedcentral.nih. bodied in Haeckel’s (1866) three-kingdom scheme, which gov/articlerender.fcgi?artid=1197417.) encompassed animals, plants, protists, and at the origin of it all, the little-understood monera, which he included in The next step: Three domains of life the protist kingdom (Figure 2). In the late 1960s, Whit- Microbiologists were never comfortable with the ill- taker (1969) included fungi in the collection and codified defined concept of monera, but also had not developed the five kingdoms that are widely taught today. a clear definition of bacteria. By the mid–20th century, The term prokaryote was coined by Chatton (1938), many leading microbiologists had lost hope for devel- who first proposed organizing life into two great “em- oping a taxonomy for bacteria based on evolutionary pires,” prokaryotes and eukaryotes (Figure 1B). His plan relationships. Instead, they had turned to shape (mor- noted differences among cell structures rather than any phology) and physiology as the basis for classification of proposed evolutionary or taxonomic differences among these organisms. But in 1977, Woese and Fox provided a the groups. Chatton’s prescient plan was rediscovered molecular means for understanding microbial relation- and made more widely known decades later by Stanier ships and evolution through comparison of ribosomal and van Neil. They defined the prokaryote as an organ- RNA sequences. Woese and Fox determined the re- ism with no nucleus or mitosis, no membrane-bound lationships of 13 representative organisms and found internal structures, and the presence of a cell wall with a that four of the supposed bacteria were, in fact, no more specific mucopeptide (1962). Many scientists questioned related to the bacteria (prokaryotes) than they were to this definition of prokaryote, which relies on negative the eukaryotes. They proposed a new taxonomic level definition (based on the absence of traits). For example, above kingdom, the “urkingdom” or primary kingdom, the simple presence or absence of traits is not sufficient in a system containing three urkingdoms: eubacteria, reason to lump flying animals such as birds, bats, and in- archaebacteria, and eukaryotae (Woese and Fox 1977). sects together; the trait of flight arose several times and Later, the urkingdoms became domains and the domain does not create an evolutionary taxonomy. Nonetheless, Archaea would be born on the sequences of these four absence became a trait, and the term prokaryote eventu- “bacteria.” Today we know that there are thousands F I G U R E 3 Biochemical characteristics of the three domains. Characteristic Domain Archaea Bacteria Eukarya Ribosome type (by sequence) Archaeal Bacterial Eukaryal Histone packing of DNA Yes No Yes Membrane-enclosed nucleus No No * Yes Membrane lipids Ether-linked Ester-linked Ester-linked Initiator tRNA Methionine Formylmethionine Methionine Operons Common Common Rare Ribosome sensitive to Yes No Yes diptheria toxin Sensitive to chloramphenicol, No Yes No streptomycin, and kanamycin Transcription promoter TATA box -10, -35 boxes TATA box Transcription initiation TATA binding protein Sigma factor TATA binding protein RNA polymerase type Pol II Pol II homolog Pol I, II, III Muramic acid in cell wall? No Yes No *Membrane enclosed nuclei have been observed in members of the planctomycetes, but these probably are not homologous to the eukaryal nuclear membrane. October 2007 49 of archaea and that they are significant contributors to a primordial beginning, at about the same time as the ge- the biosphere. This fascinating group includes the ex- netic line that led to the archaea. tremeophiles, archaea that live in the most inhospitable There are other problems with the five- or six-king- habitats on Earth. Because habitats on other planets are dom concept. First, as with the term prokaryote, monera generally extreme by Earth’s definitions, scientists expect implies a similarity between the archaea and bacteria that that extraterrestrial