A billion-years arms race between viruses and their hosts

Viruses in the kingdom Bamfordvirae make up one of the most diverse groups that infect living organisms. They include the largest viruses characterised to date (NCLDVs), viral parasites of other viruses (virophages), and adenoviruses (common viruses that cause cold and flu-like symptoms).

There are two main theories for the origins of these viruses: the ‘nuclear-escape’ and ‘virophage-first’. The nuclear-escape theory suggests that they originated within hosts and escaped from the host cell nucleus. In contrast, the virophage-first theory suggests a combination of co-evolution and later colonisation of or escape from hosts.

Researchers have proposed a new evolutionary model, suggesting a billion-years evolutionary arms race between two groups within this kingdom and their hosts. Dr José Gabriel Niño Barreat said:

Despite these proposed scenarios, the diversification of viruses in the Bamfordvirae kingdom remains a major open question in virus evolution. To gain a better understanding of their history, we wanted to test the predictions made by both the nuclear-escape and virophage-first models, and consider alternative scenarios regarding the origin of different lineages.

The researchers compared the plausibility of the evolutionary scenarios. Their analyses revealed strong evidence against the nuclear-escape theory. The findings were even somewhat at odds with a virophage-first scenario, however they do not rule it out completely – making it the one best supported by current phylogenetic analyses.

Additionally, their work supports for the positioning of the Bamfordvirae ancestral root between virophages and the other viral lineages. This pointed the team towards a new model for the evolutionary origins of these viruses. Professor Aris Katzourakis said:

The model proposes that the Bamfordvirae ancestor did not originate from an invasion of the eukaryotic cell nucleus, and that it was a non-virophage DNA virus with a small genome. The lifestyle of virophages would have evolved at a later stage as these became specialised parasites of the ancestral NCLDVs.

The relative timing of events suggests the most recent common ancestor of the Bamfordvirae kingdom existed more than a billion years ago, extending to the initial stages of eukaryotic life. Dr José Gabriel Niño Barreat added: "As well as playing important roles in Earth's ecosystems, it is becoming increasingly clear that viruses may have contributed to major evolutionary transitions during the history of life. Therefore, understanding the deep evolutionary history of viruses provides more context for these ancient interactions and the actors involved."

“Unravelling the interactions between viruses and their hosts provides a window into the deep evolutionary past that is illuminating the origins of both of these biological entities,” Professor Aris Katzourakis concludes.

To read more about this research, published in eLife, visit: https://doi.org/10.7554/eLife.86617.1