Abstract
The extension of virology beyond its traditional medical, veterinary, or agricultural applications, now called environmental virology, has shown that viruses are both the most numerous and diverse biological entities on Earth. In particular, virus isolations from unicellular eukaryotic hosts (heterotrophic and photosynthetic protozoans) revealed numerous viral types previously unexpected in terms of virion structure, gene content, or mode of replication. Complemented by large-scale metagenomic analyses, these discoveries have rekindled interest in the enigma of the origin of viruses, for which a description encompassing all their diversity remains not available. Several laboratories have repeatedly tackled the deep reconstruction of the evolutionary history of viruses, using various methods of molecular phylogeny applied to the few shared “core” genes detected in certain virus groups (e.g., the Nucleocytoviricota). Beyond the practical difficulties of establishing reliable homology relationships from extremely divergent sequences, I present here conceptual arguments highlighting several fundamental limitations plaguing the reconstruction of the deep evolutionary history of viruses, and even more the identification of their unique or multiple origin(s). These arguments also underline the risk of establishing premature high level viral taxonomic classifications. Those limitations are direct consequences of the random mechanisms governing the reductive/retrogressive evolution of all obligate intracellular parasites.
Highlights
Since the serendipitous discovery of the tobacco mosaic virus by Dmitri Ivanovsky in 1892 [1], virology has mostly focused on those viruses responsible for diseases of human, animals, or plants
One noticeable exception was the study of bacteriophages that led to the basic concepts of modern cellular biology and to many of today’s molecular biology tools [3]
A second wind of virology occurred with the discovery of the first giant viruses infecting amoeba [4,5], rapidly followed by that of an unexpected diversity of related viruses associated with other protozoan and algal hosts [6,7,8,9,10,11]
Summary
Since the serendipitous discovery of the tobacco mosaic virus by Dmitri Ivanovsky in 1892 [1], virology has mostly focused on those viruses responsible for (often dreadful) diseases of human, animals, or plants. Through isolation studies [12,13,14,15,16] complemented by large-scale environmental metagenomic explorations [17,18,19], a flurry of new viruses has since been uncovered exhibiting unexpected virion sizes and morphologies, unusual gene contents, or exotic modes of replication [12,20,21,22,23] Beyond their unanticipated diversity, these “unconventional viruses” (not to be confused with the infectious agents known as prions) [24,25]. This article will focus on even more fundamental limitations plaguing the reconstruction of the deep evolutionary history of all viruses
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