A billion years arms-race between viruses, virophages, and eukaryotes

Area of Science:

• Virology
• Evolutionary Biology
• Genomics

Background:

• Bamfordviruses represent a highly diverse viral group infecting eukaryotes, encompassing Nucleocytoplasmic Large DNA viruses (NCLDVs), virophages, adenoviruses, Mavericks, and Polinton-like viruses.
• Two primary hypotheses, 'nuclear-escape' and 'virophage-first', attempt to explain the evolutionary origins of this viral lineage.
• The 'nuclear-escape' hypothesis posits an endogenous Maverick-like ancestor originating in the nucleus, while 'virophage-first' suggests coevolution of NCLDVs with protovirophages.

Purpose of the Study:

• To rigorously test the predictions of the 'nuclear-escape' and 'virophage-first' hypotheses regarding Bamfordvirus origins.
• To explore alternative evolutionary scenarios for the diversification of this viral group.
• To elucidate the evolutionary relationships and ancient origins of major Bamfordvirus lineages.

Main Methods:

• Analysis of a comprehensive dataset comprising four core virion proteins sampled across diverse Bamfordvirus lineages.
• Application of Bayesian and maximum-likelihood hypothesis-testing frameworks.
• Estimation of rooted phylogenetic trees to infer evolutionary history and relationships.

Main Results:

• Strong evidence indicates that adenoviruses and NCLDVs are not closely related sister groups.
• The acquisition of the rve-integrase by Mavericks and Mavirus occurred independently.
• A monophyletic group of virophages (family Lavidaviridae) was identified, with the root of the Bamfordvirus phylogeny likely situated between virophages and other lineages.

Conclusions:

• The findings challenge the 'nuclear-escape' hypothesis, supporting alternative evolutionary pathways for Bamfordviruses.
• Evidence suggests a billion-year evolutionary arms race between virophages and NCLDVs.
• The study provides a refined understanding of the deep evolutionary history and interrelationships within the Bamfordvirus clade.