Abstract
Viruses can be classified into archaeoviruses, bacterioviruses, and eukaryoviruses according to the taxonomy of the infected host. The host-constrained perception of viruses implies preference of genetic exchange between viruses and cellular organisms of their host superkingdoms and viral origins from host cells either via escape or reduction. However, viruses frequently establish non-lytic interactions with organisms and endogenize into the genomes of bacterial endosymbionts that reside in eukaryotic cells. Such interactions create opportunities for genetic exchange between viruses and organisms of non-host superkingdoms. Here, we take an atypical approach to revisit virus-cell interactions by first identifying protein fold structures in the proteomes of archaeoviruses, bacterioviruses, and eukaryoviruses and second by tracing their spread in the proteomes of superkingdoms Archaea, Bacteria, and Eukarya. The exercise quantified protein structural homologies between viruses and organisms of their host and non-host superkingdoms and revealed likely candidates for virus-to-cell and cell-to-virus gene transfers. Unexpected lifestyle-driven genetic affiliations between bacterioviruses and Eukarya and eukaryoviruses and Bacteria were also predicted in addition to a large cohort of protein folds that were universally shared by viral and cellular proteomes and virus-specific protein folds not detected in cellular proteomes. These protein folds provide unique insights into viral origins and evolution that are generally difficult to recover with traditional sequence alignment-dependent evolutionary analyses owing to the fast mutation rates of viral gene sequences.
Highlights
Depending on the nature of the infected host, viruses can be broadly classified into three major groups, archaeoviruses, bacterioviruses (Krupovic et al, 2016), and eukaryoviruses, in addition to the lesser-known virophages that parasitize giant viruses (La Scola et al, 2003, 2008)
Based on the presence/absence of these viral fold superfamilies (FSFs) in 1,620 cellular proteomes from Archaea (122 in number), Bacteria (1,115), and Eukarya (383), seven mutually exclusive Venn groups could be defined each for archaeoviruses, bacterioviruses, and eukaryoviruses: A, B, E, AB, AE, BE, and ABE, in addition to virusspecific (V) FSFs not detected in cellular proteomes (Figure 2)
A simple comparative genomic analysis calculating the spread of viral protein domain structure FSFs in reported host and non-host cellular proteomes revealed that proteomes of virus hosts harbored several viral hallmark proteins necessary for virion assembly and successful viral infection cycles (Table 1)
Summary
Depending on the nature of the infected host, viruses can be broadly classified into three major groups, archaeoviruses, bacterioviruses (Krupovic et al, 2016), and eukaryoviruses, in addition to the lesser-known virophages that parasitize giant viruses (La Scola et al, 2003, 2008). While host jumps are common (Longdon et al, 2014; Geoghegan et al, 2017), such as HIV from chimps (Sharp and Hahn, 2010), SARS Coronavirus from bats (Li et al, 2005), H1N1 from birds (Webby and Webster, 2001), and arboviruses that replicate in mammalian cells and insect vectors, viruses are not known to infect cellular organisms separated by superkingdom (domain of life) boundaries (Nasir et al, 2014, 2017). Host-constrained evolution of viral lineages has led to favoring either the “escape” or “reduction” models for the origin of modern viruses, both attributing viral origins from modern or ancient host cells (reviewed in Hendrix et al, 2000; Forterre and Krupovic, 2012; Nasir et al, 2012b)
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