New Evolutionary Model for the Origin of Kingdom of Viruses: Bamfordvires

Their study, published today as a Reviewed Preprint in eLife, provides what the editors say are compelling analyzes that advance our understanding of the deep evolutionary history of viruses, the interaction between viruses and early eukaryotes (organisms with cells that include a nucleus), and the diversification of viral lines.

Viruses in the Kingdom Bamfordvires are one of the most diverse groups that infect living organisms. They include nucleocytoplasmic large-DNA viruses (NCLDV, the largest viruses characterized to date), virophages (viral parasites of other viruses), adenoviruses (common viruses that cause cold and flu symptoms), and Mavericks and Polinton-like viruses (the two virus-like mobile genetic elements that colonize the genomes of their hosts).

There are two main hypotheses for the origins of these viruses: the “nuclear escape” and “virophage first” hypotheses. The nuclear escape hypothesis says that a Maverick-like ancestor was born with hosts (endogenous), escaped from the host cell nucleus and gave rise to adenoviruses and NCLDVs. In contrast, the virophage-first hypothesis suggests that NCLDVs co-evolved with early virophages. Mavericks then evolved from virophages that became endogenous, with adenoviruses escaping from the host nucleus at a later stage.

“Despite these proposed scenarios, the diversification of viruses in the Bamfordvires kingdom remains a major open question in the evolution of viruses. To better understand their history, we wanted to test the predictions made by both nuclear escape and virophage models first, and consider alternative scenarios regarding the origin of the different lineages,” explains José Gabriel Niño Barreat, A postdoctoral research assistant at Barreat is co-author of the study alongside Aris Katzourakis, professor of evolution and genomics in the department of biology at the University of Oxford.

Barreat and Katzourakis used two hypothesis testing methods (maximum likelihood and Bayesian frameworks) to compare the plausibility of nuclear escape against alternative evolutionary scenarios. They focused on four key proteins shared by viruses of this lineage that are involved in the formation of viral capsids: major and minor capsid proteins, DNA packaging ATPase and protease. They applied two other methods that use genetic data to estimate rooted phylogenies, to infer the evolutionary trajectory of different lineages. Next, they assessed whether adenoviruses and NCLDV descended from a common ancestor, as predicted by the nuclear escape scenario.

Their analyzes revealed strong evidence against a sister relationship between adenoviruses and NCLDVs, as suggested by the nuclear escape hypothesis. Instead, the results suggest that adenoviruses are descended from a common ancestor with Mavericks, excluding NCLDV. Contradicting a virophage-first scenario, researchers found that the most recent common ancestor of Mavericks and adenoviruses were not virophages. However, their work does not completely rule out the virophage-first hypothesis, making it the best supported by current phylogenetic analyses.

In addition, their work provides support for the positioning of the Bamfordvires ancestral root between virophages and other viral lineages. This positioning directed the team towards a new model of the evolutionary origins of these viruses.

“The model proposes that the Bamfordvires the ancestor did not come from an invasion of the eukaryotic cell nucleus, and that it was a non-virophage DNA virus with a small genome,” explains co-author Aris Katzourakis. “The lifestyle of virophages would have evolved at a later stage as they became specialized parasites of ancestral NCLDVs.” Katzourakis adds that the relative chronology of events suggests the most recent common ancestor of Bamfordvires kingdom existed more than a billion years ago, extending to the initial stages of eukaryotic life. However, an absolute time scale for the precise dating of these events is not currently available.

Another limitation of the study is that the phylogenetic signal in the analyzed protein data may have been obscured by the deep divergences and extreme diversity of this lineage. However, the authors were able to make a strong distinction between the alternative scenarios, and the focus on the origin and development of the viral capsid provides a straightforward way to explain the available data.

“This work contributes to our knowledge of how viruses develop different evolutionary strategies, for example to become parasites of other viruses like virophages, or viral giants like NCLDVs,” says Barreat. “In addition to playing important roles in Earth’s ecosystems, it is becoming increasingly clear that viruses may have contributed to major evolutionary transitions throughout the history of life. Therefore, understanding the deep evolutionary history of viruses provides more context for these ancient interactions and the actors involved.”

“Unraveling the interactions between viruses and their hosts opens a window into the deep evolutionary past that sheds light on the origins of these two biological entities,” concludes Katzourakis.