The Simplest of Eukaryotic Cells

fibrillanosema_sporeMicrosporidia are intracellular parasites that infect most other eukaryotic cells, although arthropods are the most commonly parasitized. They are the simplest and smallest eukaryotic cells and thus represent a textbook example of reductive evolution [1]. Whereas scientists once classified microsporidia as protozoa, it is now generally recognized that they are highly evolved fungi. A more extensive discussion of their biology can be found here.

This simple fungus an important lesson to teach us.

In the 1980s, scientists viewed microsporidia as the most primitive example of a eukaryote. How is it they mistakenly viewed a highly evolved fungus for a primitive protozoan? In their review [2], Patrick J. Keeling and Naomi M. Fast explain the situation as follows:

However, in 1983, attention was drawn to the possible evolutionary significance of microsporidia in a new way. Cavalier-Smith proposed that the origin of eukaryotes might have preceded the endosymbiotic origin of the mitochondrion by some considerable span of time, implying that there may be protists that evolved before the mitochondrial origin. In other words, there may be primitively amitochondriate eukaryotes, and focusing attention on these protists could unlock some of the secrets surrounding the origin of eukaryotes. Four lineages of amitochondriate protists that could hold this pivotal position were identified, and these were collectively named Archezoa: Archamoebae (e.g., Entamoeba), Metamonada (e.g., Giardia), Parabasalia (e.g., Trichomonas), and Microsporidia.

Lev Seravin, from the Biological Research Institute of St. Petersburg State University, recounts how Cavalier-Smith has to quickly dismantle Archezoa soon after establishing it [3]. He explains why Cavalier-Smith introduced this classification scheme:

Proceeding from a fairly widely spread point of view that the simpler the living organisms the more originally primitive they should be, he united the macrotaxa including the flagellates and amoeboid organisms devoid of mitochondria into a single subkingdom Archezoa as a phylogenetically initial state for all the rest of the Protozoa kingdom.

Clearly, Cavalier-Smith was misled by the assumption that “simple = primitive.” Nevertheless, and here is the key point, there was a very impressive list of evidence that supported Cavalier-Smith’s classification.

I already mentioned that microsporidia are the smallest and simplest eukaryote. They not only lack mitochondria, but also lack other widely distributed eukaryotic organelles such as flagella, golgi bodies, and peroxisomes. So it would appear that microsporidia branched off the eukaryotic tree prior to the emergence of these organelles. This hypothesis was supported by more scientific discoveries

1. Their genomes can be smaller than those of bacteria. For example, one species of microsporidia has a genome with 2.3 million nucleotides, while E. coli‘s genome is around 4.6 million nucleotides [1].

2. What was even more remarkable was the bacterial-like ribosome of microsporidia. The eukaryotic ribosome is known as the 80S ribosome (a rough measure of its size), while bacteria possess 70S ribosomes. Microsporidia have 70S ribosomes, meaning that their ribosomes are about the same size as those found in bacteria. And what’s even more striking is that their 5.8S rRNA and 28S rRNA are fused. This is what we see in bacteria. This fusion occurs at the level of the rRNA genes, again as in bacteria.

3. Then the case got even stronger:

Shortly after the Archezoa hypothesis was formulated, the tools of molecular phylogenetics began to be applied vigorously to microbial eukaryotes, and the first molecular data from microsporidia lent extraordinary support to the Archezoa hypothesis. The small subunit ribosomal RNA (SSU rRNA) from the microsporidian Vairimorpha was shown to be the earliest branch on the eukaryotic tree, and of greater interest, the microsporidia were found to be the only eukaryotes to retain the prokaryotic trait of having their 5.8S rRNA fused to the large subunit (LSU) rRNA. These two pieces of evidence bolstered the notion that microsporidia were indeed an ancient and primitive lineage, and further evidence seemed to accumulate with the sequencing of every new microsporidian gene: Phylogenies based on elongation factor 1alpha, elongation factor 2, as well as isoleucyl tRNA synthetase, all showed the microsporidia branching deeply.

The same apparent early phylogenetic position was also seen with other Archezoa (with the possible exception of Entamoeba), and altogether the case of an ancient origin and primitive lack of mitochondria for microsporidia and other Archezoa seemed neatly sewn up. [2]

Yet it was all wrong. A closer analysis of the microsporidian genome found evidence of many mitochondrial genes. And a closer look at genes for tubulin, elongation factors, heat shock proteins, and the RNA polymerase, found that microsporidia clustered with fungi (see here for example). As of today, most scientists (including Cavalier-Smith) reject the existence of Archezoa and recognize microsporidia as highly derived parasitic fungi.

This piece of scientific history carries a clear lesson – we should always be careful to recognizing the tentative nature of our hypotheses. If a hypothesis as well supported as the microsporidia-as-primitive-protozoan hypothesis can be wrong, then just because a hypothesis is supported by an impressive list of evidence does not mean it is correct.

I have little doubt that if people were blogging in the 1980s, we’d have plenty of archived material where people were proclaiming microsporidia as primitive protozoa while berating those who were skeptical. So look at it this way. Is your position as well-supported as the microsporidia-as-primitive-protozoan hypothesis was in the 1980s? Don’t be so cocky, as there is a good chance it could still be wrong.

1. Andersson SG, Kurland CG. 1998. Reductive evolution of resident genomes. Trends Microbiol6:263-8.

2. Keeling, PJ and Fast, NM. 2002. MICROSPORIDIA: Biology and Evolution of Highly Reduced Intracellular Parasites. Annu. Rev. Microbiol. 56:93″“116.

3. Seravin, LN. 2001. The principle of counter-directional morphological evolution and its significance for construction the megasystem of protists and other eukaryotes. Protistology 2:6-14.

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