The Three Domain System

First, I would appreciate if you allow me a bit of retrospective. I went through high school in the late eighties and graduated college in the mid nineties. I thoroughly enjoyed my biology courses (honors in high school). We were taught many things, unfortunately mostly by rote. Later, during my stint as a science teacher (in the mid 2000s), I had the opportunity to share with my students how science could change over time. One of the things we discussed was a change caused by the paper I’m about to talk about it.

On the surface, this paper seems like such a basic concept. Indeed, the paper itself only has 33 references. However, it really changed a lot of how we looked at the world.

C R Woese, O Kandler, and M L Wheelis. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya PNAS 1990 87 (12) 4576-4579
http://www.pnas.org/content/87/12/4576.full.pdf+html

Abstract
Molecular structures and sequences are generally more revealing of evolutionary relationships than are classical phenotypes (particularly so among microorganisms). Consequently, the basis for the definition of taxa has progressively shifted from the organismal to the cellular to the molecular level. Molecular comparisons show that life on this planet divides into three primary groupings, commonly known as the eubacteria, the archaebacteria, and the eukaryotes. The three are very dissimilar, the differences that separate them being of a more profound nature than the differences that separate typical kingdoms, such as animals and plants. Unfortunately, neither of the conventionally accepted views of the natural relationships among living systems–i.e., the five-kingdom taxonomy or the eukaryote-prokaryote dichotomy–reflects this primary tripartite division of the living world. To remedy this situation we propose that a formal system of organisms be established in which above the level of kingdom there exists a new taxon called a “domain.” Life on this planet would then be seen as comprising three domains, the Bacteria, the Archaea, and the Eucarya, each containing two or more kingdoms. (The Eucarya, for example, contain Animalia, Plantae, Fungi, and a number of others yet to be defined). Although taxonomic structure within the Bacteria and Eucarya is not treated herein, Archaea is formally subdivided into the two kingdoms Euryarchaeota (encompassing the methanogens and their phenotypically diverse relatives) and Crenarchaeota (comprising the relatively tight clustering of extremely thermophilic archaebacteria, whose general phenotype appears to resemble most the ancestral phenotype of the Archaea.
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Linnaeus started the whole ‘classification’ thing by placing all organisms into one of two groups: Plants and Animals. It went this way for a long time, then Stanier popularized the concept of including bacteria in their own group (prokaryotes, versus the eukaryotes of plants and animals). [1]

In 1969, Robert Whittaker published the idea of using evolutionary relationships as the basis for classifying organisms into similar categories. This results in the Five Kingdom System that biology students in my day were so familiar with: Animal, Plant, Fungus, Monera (bacteria), and Protist (which is where something went if it didn’t really fit into the other four). [2] This was a pretty effective system, until advances in molecular biology came along and we realized that all those bacteria that look the same… weren’t.

In 1980, Carl Woese (the future author of the paper I’ll be describing in a moment) pushed a classification scheme with an emphasis on the evolutionary relationships and redefined the kingdoms to consist of an ancestor organism and all of it’s descendents (the key word here is ‘all’, this concept is called a monophyletic group and is a very important grouping in cladistics). At this point, Woese broke the prokaryotes (Kingdom Monera) into two kingdoms: Eubacteria and Archaebacteria. This met with some success.

Woese also attempted to combine all the eukaryote kingdoms in one kingdom. This met with much less success. However, he persisted with the concept and in 1990, published a paper with the sub-title “proposal for the domains Archaea, Bacteria, and Eucarya”.

Woese begins by describing the 1980s as the time when biologists could begin to “trace the evolutionary history of organisms back to the most recent common ancestor of all life”. Molecular biology began to show scientists much more detail about the evolutionary relationships of organisms than traditional techniques (like comparative anatomy) could show. This was especially important for the bacteria. There are three broad categories for bacteria, rod-shaped, sphere-shaped, and spiral-shaped. This was not very useful for determining how these organisms were related (or not related).
Woese felt that the time had come to develop a classification system that took this new information into account. The current system had its good points, but was woefully inadequate for some things.

Imagine, if you will, that you are a carpenter, a good one. You have your nails organized by size, weight, and material (galvanized for outdoors). You have hundreds of buckets for each and every nail type you ever used. You can find the exact nail for any project in seconds with your system. One day a neighbour asks for a bolt to hold two pieces of metal together. You open a drawer at the bottom of your cabinet and there are thousands of bolts, nuts, and screws all jumbled into one big mass.

That was the state of classification around the time the Woese article was written. Plants, animals? No problem. Even the odd protist wasn’t very difficult to place. But all these bacteria? Just a single junk drawer existed for all of them.

The problem was that there wasn’t a sound basis for any of the kingdoms. It all started with Linnaeus and no one saw fit to change it. Animals and plants had some physical characters, but molecularly speaking they were the same thing. Evolutionarily speaking, eukaryotes existed for a billion years before organisms that fit what we know of as ‘plants’ and ‘animals’ existed. [This is kind of like dividing coins by giving more weight to their printing location rather than their value, date, or material makeup.]

According to Woese, protists and fungus are in even worse shape. These are completely made up categories. I mentioned that Kingdom Protist is basically the dumping ground for organisms that do not fit into other categories. A protist can be single or multi-celled (though simple), a heterotroph or autotroph, and sexual or asexual.

Finally, of course, was Kingdom Monera. These organisms are so different from all the other kingdoms. They do not have any membrane bound organelles (generally). They store their DNA in a single loop rather than unconnected chromosomes. There are many other differences, but these will do for us.

In fact Woese states “the differences between Monera (prokaryotes) and the four other kingdoms are far more significant, and of a qualitatively different nature, than the differences among these four. In other words, a primary division of life must lie between the bacteria and the eukaryotic forms; the animal/plant distinction is definitely secondary.”

What is really interesting and the basis for Woese’s 3 Domain system is that the two groups of prokaryotes (Eubacteria and Archaebacteria) are almost as fundamentally different from each other as either is from Eukarya. This could be traced through the evolutionary lineage of each group.

Archaebacteria are (arguably) the original life form on Earth. Archae generally live in extreme environments, hot springs, toxic waste, nuclear reactors, and other places that would kill most ‘normal organisms’. These organisms contain unique lipid structures that (again, arguably) place them in existence 2.7 billion years ago. [4] [5] Perhaps most interestingly, archaebacteria contain several genes and metabolic pathways that actually make them seem more like eukaryotes than eubacteria.

Eubacteria are the bacteria that we normally think of when someone mentions bacteria. These are the organisms that live on our skin and in our guts, both useful and harmful. Research suggests that eubacteria and archaebacteria had a common ancestor 2.5 to 3.2 billion years ago. [6][7] “All eubacteria, for example, exhibit nearly the same subunit pattern (in terms of numbers and sizes) in their RNA polymerases; however, this pattern bears little relationship to that seen in either the archaebacteria or the eukaryotes.”

Eukaryotes are… well… us. These organisms have some unique structures not found in the other two groups. There are membrane bound organelles like the nucleus and mitochondria and a unique arrangement of DNA and some very special molecular components.

Woese’s new classification system was based in these three most fundamental categories: Eubacteria, Archaebacteria, and Eukaryotes. He claimed that these fundamental differences must stand above the present (at the time) Kingdoms. Woese did recognize that it would be effectively impossible to change the kingdoms as they existed at the time. Even toddlers who can barely walk know the difference between plant and animal. However, Woese thought that he could introduce a layer of classification above the kingdom that would properly divide all organisms into groups based on molecular and evolutionary history. Not just how the organism looked and what it ate.

So Woese proposed the Three-Domain system. In which all living things would be Archaebacteria, Eubacteria, or Eukarya.

Finally, in introducing the domain Archaebacteria, Woese suggested two ‘kingdom’ level classifications to start the classification of Archaebacteria.

This was to be a fundamental revision to a classification system that had existed more-or-less the same for over 200 years. This concept was not accepted immediately by the scientific community at large. My understanding is that some of the great names in biology (including Ernst Mayr) were heavily opposed to this revision. However, by the mid 1980s, the concept had become more accepted by scientists and by 2002, the Three-Domain System was accepted to the point where high school level text-books were using it.

I admit, I wasn’t too impressed when I saw the Three-Domain System for the first time. I thought it unnecessary additions to a perfectly good classification system. In fact, I would have (and still would) liked a major revision of Kingdom Protist. However, I too have become convinced by the molecular and evolutionary data that this system makes sense at the highest level.

At present, there is no need for another ‘dumping ground’ (like Protist) at the Domain level. Every organism must fit into one of the three domains, naturally, based on uncontroversial molecular information. Some scientists (myself included) have used this system as a basis for speculation regarding life on other worlds and how bacteria (Eubacteria) must be very well evolved for a non-extreme environment and how Archaebacteria may contain the ancestor of all life on this planet and on other planets.

It’s a simple, but profound concept.
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references
Woese, C. (1990). Towards a Natural System of Organisms: Proposal for the Domains Archaea, Bacteria, and Eucarya Proceedings of the National Academy of Sciences, 87 (12), 4576-4579 DOI: 10.1073/pnas.87.12.4576

[1] Stanier RY, Van Niel CB (1962). “The concept of a bacterium”. Archiv Für Mikrobiologie 42: 17–35. PMID 13916221.

[2] Whittaker RH (January 1969). “New concepts of kingdoms or organisms. Evolutionary relations are better represented by new classifications than by the traditional two kingdoms”. Science 163 (863): 150–60. PMID 5762760. http://www.sciencemag.org/cgi/pmidlooku … id=5762760.

[3] Wang M, Yafremava LS, Caetano-Anollés D, Mittenthal JE, Caetano-Anollés G (2007). “Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world”. Genome Res. 17 (11): 1572–85. doi:10.1101/gr.6454307. PMID 17908824.

[4] Brocks JJ, Logan GA, Buick R, Summons RE (1999). “Archean molecular fossils and the early rise of eukaryotes”. Science 285 (5430): 1033–6. doi:10.1126/science.285.5430.1033. PMID 10446042.

[5] Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR (October 2008). “Reassessing the first appearance of eukaryotes and cyanobacteria”. Nature 455 (7216): 1101–4. doi:10.1038/nature07381. PMID 18948954.

[6] Di Giulio M (2003). “The universal ancestor and the ancestor of bacteria were hyperthermophiles”. J Mol Evol 57 (6): 721–30. doi:10.1007/s00239-003-2522-6. PMID 14745541.

[7] Battistuzzi FU, Feijao A, Hedges SB (November 2004). “A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land”. BMC Evolutionary Biology 4: 44. doi:10.1186/1471-2148-4-44. PMID 15535883.