Do Viruses Exchange Genes across Superkingdoms of Life?

Malik, Shahana S.; Azem-e-Zahra, Syeda; Kim, Kyung Mo; Caetano-Anollés, Gustavo; Nasir, Arshan

The comparative exercise of tracing the spread of each viral FSF in cellular proteomes was made explicit with an f -value representing the fraction of cellular proteomes encoding individual FSFs (see Methods). The f -values of viral FSFs in cellular proteomes and their reported biochemical functions were then used to postulate hypotheses regarding the direction of gene transfer, virus-to-cell or cell-to-virus (see Figure 1 for demonstration). For example, an FSF with a viral hallmark function (e.g., virion synthesis) that had negligible presence in proteomes of a cellular superkingdom (e.g., f < 1%) was considered a candidate for horizontal gene transfer (HGT) event from virus-to-cell rather than from cell-to-virus as the latter would require invoking multiple gene loss events in related cellular species. This approach of inferring the likely direction of gene transfer is thus similar to considering anomalous phylogenetic distributions of genes in closely related species as more likely a result of HGT rather than vertical inheritance and loss. This method reliably detects HGT events (Philippe and Douady, 2003) , especially in viral genes where sequence identity with cellular counterparts may be too low to produce meaningful alignment-dependent phylogenetic trees (Nasir and Caetano-Anollés, 2015) . The tracings yielded unique insights into genetic transfers between viruses and cells, highlighted the quantitatively greater cross-superkingdom genetic exchange occurring between bacterioviruses and eukaryotes and eukaryoviruses and bacteria, and supported models of viral origins from ancient cells (Nasir et al., 2012b) . The genetic crosstalk between viral and cellular proteomes that we uncover with this comparative genomics FIGURE 1 | Demonstration of virus-to-cell and cell-to-virus HGT events. Ten genomes are displayed as colored closed disks each for Archaea (black), Bacteria (blue), Eukarya (green), and viruses. Seven out of 10 viral genomes encode different virus hallmark FSFs (with incidence represented by different shades of red) such as those involved in virion synthesis and capsid assembly. If any of these virus-hallmark FSFs is detected in no more than 1/10 cellular genomes (real f-values are even lower), the event is determined to be virus-to-cell HGT. In turn, any of the cellular FSFs that are widespread in cells (i.e., present in 9/10 cellular genomes) are detected in a viral genome, that event is determined to be cell-to-virus HGT. approach presents a more global picture for evolutionary understanding of virus-cell interactions that goes beyond the perceived textbook definitions of virus hosts .