Organization and evolution of the virosphere and the replicator space

Viruses are obligate symbionts of cellular life forms that can replicate only within host cells and typically form virions (virus particles) to spread among host organisms. Virions numerically dominate the biosphere, exceeding the number of cells several-fold, and also comprise the main reservoir of genetic diversity on earth. Nearly all organisms host multiple, diverse viruses. Unlike cellular organisms, viruses have genomes (genetic information carriers incorporated into virions) that consist of all forms of RNA and DNA, suggesting an evolutionary connection between extant viruses and the primordial replicator pool. Lately, extensive mining of metagenomes and metatranscriptomes has dramatically expanded the world of viruses (virosphere), revealing an unsuspected and unprecedented diversity. Viruses share no universal genes and have multiple origins. However, about 15 viral hallmark genes each bring together multiple, diverse groups of viruses, and many other genes are shared within such groups. Evolution of viruses is inextricably intertwined with the evolution of their hosts. A key aspect of virus-host coevolution is the arms race resulting in accelerated evolution on both sides, especially of host defenses and viral counter-defenses. A complementary, prominent feature of this coevolution is exaptation, whereby viral genes are coopted by the hosts for antiviral defense and other roles, and conversely, viruses capture host genes for diverse functions in virus replication, virion morphogenesis and virus-host interaction. In this review, we attempt a synthesis of the current understanding of the global organization of the virosphere, the major trends and events in the evolution of viruses, and the high-level taxonomy of viruses.