Three Domains of Life: Woese's Phylogenetic Revolution

Paper Information

Citation: Woese, C. R., Kandler, O., & Wheelis, M. L. (1990). Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA, 87(12), 4576-4579. https://doi.org/10.1073/pnas.87.12.4576

Publication: Proc. Natl. Acad. Sci. USA 1990

Additional Resources:

• Woese’s 1977 Discovery of Archaea
• NCBI Taxonomy Browser

What kind of paper is this?

This is a Systematization paper with a strong Position component.

Systematization: It synthesizes decades of molecular sequence data (specifically rRNA) to propose a “formal system of organisms” that replaces previous taxonomies.

Position: It aggressively argues that the prevailing “Prokaryote-Eukaryote” and “Five Kingdom” models are “outmoded,” “misleading,” and based on “flawed premises” regarding the organization of life.

What is the motivation?

The authors aim to align formal taxonomy with the “natural system emerging from molecular data”.

The Problem: Existing systems (Whittaker’s 5-Kingdoms) were based on morphology and nutrition, which are insufficient for microbial classification.

The Gap: The “Prokaryote” definition was negative (defined by what they lack - a nucleus), obscuring the fact that “Archaebacteria” are as distinct from “Eubacteria” as they are from Eukaryotes.

The Goal: To establish a taxonomic rank above Kingdom that recognizes the three primary evolutionary lineages.

What is the novelty here?

The core contribution is the formal proposal of the Domain as the highest taxonomic rank. Specific novel definitions include:

1. Three Domains:

   • Bacteria (formerly Eubacteria): Membrane lipids are diacyl glycerol diesters; eubacterial rRNA.
   • Archaea (formerly Archaebacteria): Membrane lipids are isoprenoid glycerol diethers/tetraethers; archaeal rRNA. The term “archaebacteria” is abandoned to emphasize their independence.
   • Eucarya (Eukaryotes): Cells with nuclei; ester lipids; eukaryotic rRNA.

2. Subdivision of Archaea: The domain is formally split into two kingdoms:

   • Euryarchaeota (methanogens, halophiles, thermoplasms).
   • Crenarchaeota (sulfur-dependent extreme thermophiles).

What experiments were performed?

This paper is a synthesis of phylogenetic analysis rather than a report of new wet-lab experiments. It relies on:

• rRNA Sequencing: Comparison of 16S (small subunit) ribosomal RNA sequences from over 400 organisms.
• Phylogenetic Tree Reconstruction: Analysis of branching orders and lengths based on rRNA sequence comparisons (citing Woese, 1987).
• Paralogous Gene Rooting: Determining the root of the universal tree by comparing duplicated genes (e.g., elongation factors) that diverged before the three lineages separated.

What were the outcomes and conclusions drawn?

• Tripartite Division: Life divides into three monophyletic groups, not two. The distance between Bacteria and Archaea is greater than between plants and animals.
• Archaea-Eucarya Sisterhood: The root of the tree separates Bacteria from the other two, making Archaea and Eucarya sister groups.
• Molecular Definition: Phenotypes are replaced by molecular signatures. For example, Bacteria are defined by a 6-nucleotide bulge in the 16S rRNA (positions 500-545), whereas Archaea and Eucarya share a 7-nucleotide bulge.

Reproducibility Details

Note: As a theoretical systematics paper from 1990, “reproducibility” refers to the data sources and criteria used to construct the taxonomy.

Data

The taxonomy rests on comparative analysis of Ribosomal RNA (rRNA), specifically the small subunit (16S in prokaryotes, 18S in eukaryotes).

Algorithms

The paper implicitly relies on the phylogenetic methods standard at the time (Distance Matrix methods) to generate the universal tree in Figure 1.

• Tree Inference: Branching order/lengths taken from Microbiol. Rev. 51, 221-271 (1987).
• Rooting Strategy: The “Outgroup” method using anciently duplicated genes (paralogs) such as Elongation Factors Tu and G, which diverged prior to the Universal Ancestor.

Models

The “Model” proposed is the Three-Domain System:

1. Domain Bacteria: Rooted independently. Includes Thermotogales, Flavobacteria, Cyanobacteria, Purple bacteria, Gram-positives, Green nonsulfur.
2. Domain Archaea:
   • Kingdom Crenarchaeota: “Ancestral” phenotype (thermophily). Includes Pyrodictium, Thermoproteus.
   • Kingdom Euryarchaeota: “Broad” phenotype. Includes Methanogens, Halophiles, Thermoplasma.
3. Domain Eucarya: Includes Animals, Ciliates, Plants, Fungi, Flagellates, Microsporidia.

Evaluation

The authors validate the model by demonstrating Molecular Invariants - features present in all members of a domain but absent in others:

Citation

@article{woeseNaturalSystemOrganisms1990,
  title = {Towards a Natural System of Organisms: Proposal for the Domains {{Archaea}}, {{Bacteria}}, and {{Eucarya}}.},
  shorttitle = {Towards a Natural System of Organisms},
  author = {Woese, C R and Kandler, O and Wheelis, M L},
  year = {1990},
  month = jun,
  journal = {Proceedings of the National Academy of Sciences of the United States of America},
  volume = {87},
  number = {12},
  pages = {4576--4579},
  issn = {0027-8424},
  doi = {10.1073/pnas.87.12.4576}
}