Australian biologist emphasizes role viruses may have played in origin of eukaryotes

Eukaryotes are organisms with a separate nucleus containing the genetic material, a protein-transcribing apparatus in the cytoplasm, and energy-producing organelles such as mitochondria.

Cells with these features are thought to have evolved about 1.8 billion years ago. Simpler organisms such as the bacteria and archaea, known as prokaryotes, are thought to have already been around for nearly 2 billion years when eukaryotes emerged.

For a long time, supporters of the theory of evolution supposed that all life descended from a single universal common ancestor and new classes of organisms diverged from it like the branches on a tree trunk. A problem with this theory, however, is that there is a huge gap between the physiological features of prokaryotes and eukaryotes and no clear line in between. 

An alternative to the universal common ancestor theory dates back to the end of the 19th Century, when different European biologists proposed that some current organisms derived from symbioses of distinct organisms. A school of Russian botanists proposed that the lichens, which are a symbiosis between a green alga and a fungus, served as a model for the evolution of chlorophyl-containing plants. 

In 1967, American biologist Lynn Sagan (Margulis) published a paper proposing three organelles in eukaryotic cells––mitochondria, chloroplasts, and the basal bodies involved in mitosis––were once free-living prokaryotic cells that combined with primitive eukaryotic cells in a symbiotic relationship.

Although Margulis’ work was ignored or rejected at first, her view of eukaryotic origins, known as endosymbiosis, was adopted and advanced by others. Key questions that remained included how the primitive eukaryotic host organism came to be, and why such a vast chasm exists between prokaryotic and eukaryotic cells in respect to design, function, and apparent lineage. 

Viral eukaryogenesis according to Bell

Philip J.L. Bell, a microbiologist who now runs a biotech company in Australia, proposed a new conception as far back as 2001 which he called viral eukaryogenesis. A paper by Bell updating his hypothesis with consideration of many new discoveries appears May 11 in the online journal Frontiers in Microbiology. 

According to Bell, the birth of the eukaryotic cell involved the combination of three already existing biological components, including

• An Asgard archaeon, which may be the origin of the cell cytoplasm.

• A DNA virus, the probable origin of the eukaryotic nucleus. 

• An alpha-protoeobacterium related to the modern Rickettsia genus, which is the probable origin of the mitochondrion. 

Four phases of development

Bell speculates about the possible stages of development these three components might have undergone.

In Phase 1 of eukaryogenesis, the Asgard archaeon is infected by a virus, probably related to the tectiviruses, resulting in formation of a virocell. The virocell is a recent concept that describes the situation where a virus has infected and partially taken over the genetic apparatus of a host. 

The “viral factory” within the virocell produces a separation of transcription (gene copying) from translation (protein assemblage from a gene copy), a feature that distinguishes eukaryotes from prokaryotes such as bacteria. The virocell also introduces two other eukaryotic features, an endomembrane system and a dynamic cytoskeleton. 

In Phase 2, a bacterium of the class Alphaproteobacteria evolves the ability to infect the virocell through the same system of vesicles that has allowed the tectivirus to chronically infect the archaeal host. Within this phase, Bell says “the rare and defining step of eukaryogenesis” occurs when the viral factory “enslaved” one of the bacterial parasites “converting the virocell into a three-component super-organism with emergent properties.” 

The enslaved bacterium is then able to produce energy and raw materials to sustain the viral factory in a symbiotic relationship, like a chloroplast or mitochondrion in the modern eukaryotic cell.

In Phase 3, “there is a continuing transfer of genes from the enslaved endosymbiont to the viral genome as it takes over complete control of the endosymbiont’s metabolism,” Bell said. “A similar process results in the transfer of a complete translation apparatus and basic metabolism from the host archaeon to the viral genome.”

By the time it has evolved into the last eukaryotic common ancestor (LECA), “only 69 genes remain in the endosymbiont genome, and the archaeal host genome is completely lost, resulting in a protozoan-like eukaryotic predator,” Bell argues.

In the final Phase 4, the super-organism has evolved into an amoeba-like predator, possessing a new feature not previously seen––sexual reproduction. This leads to “an evolutionary arms race selecting for larger and more complex eukaryotic organisms resulting in the evolution of the diverse range of eukaryotes observed today,” Bell proposes.

He believes that the wide distribution of mitosis, meiosis, and sexual reproduction among eukaryotes suggests these features developed from the earliest eukaryotic cells.

Darwin’s ‘Tree of Life’

Endosymbiosis poses a challenge to Darwin’s original view of evolution in which small changes in existing organisms, by a process of natural selection, eventually produce the changes that give rise to new species and phenotypes. If instead there are sudden jumps (saltations) caused by symbiotic combination, then the “tree of life” metaphor cannot easily explain evolutionary history. This was one reason that early proposals of endosymbiosis were rejected. 

Bell believes that Darwin’s characterization of a “tree of life” with a “last universal common ancestor” (LUCA) has validity after the eukaryotic domain emerged. However it cannot explain its origin, nor account for the other domains of viruses, bacteria, and archaea, which Darwin knew little, or nothing, about.

As Bell writes in his concluding paragraph: 

“Finally, it should be noted that Darwin applied his theory of natural selection to members of the eukaryotic domain, almost exclusively plants and animals. Unlike the contested relationship between viruses, bacteria, archaea and eukaryotes, there is mounting evidence that all modern eukaryotes descend from a single Last Eukaryotic Common Ancestor, and thus, all eukaryotes can and should be placed on a single eukaryotic Tree of Life. Since Darwin was essentially ignorant of bacteria, his assumption that all the organisms with which he was familiar descended from a common ancestor via the process of natural selection has essentially been vindicated, and as he intuited over 150  years ago, their evolutionary relationships are best described in a tree-like fashion.”

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Philip J.L. Bell. Eukaryogenesis: The Rise of an Emergent Superorganism. Front. Microbiol. 13:858064. (2022).

DOI: https://doi.org/10.3389%2Ffmicb.2022.858064