Abstract
Jumbo phages have attracted much attention by virtue of their extraordinary genome size and unusual aspects of biology. By performing a comparative genomics analysis of 224 jumbo phages, we suggest an objective inclusion criterion based on genome size distributions and present a synthetic overview of their manifold adaptations across major biological systems. By means of clustering and principal component analysis of the phyletic patterns of conserved genes, all known jumbo phages can be classified into three higher-order groups, which include both myoviral and siphoviral morphologies indicating multiple independent origins from smaller predecessors. Our study uncovers several under-appreciated or unreported aspects of the DNA replication, recombination, transcription and virion maturation systems. Leveraging sensitive sequence analysis methods, we identify novel protein-modifying enzymes that might help hijack the host-machinery. Focusing on host–virus conflicts, we detect strategies used to counter different wings of the bacterial immune system, such as cyclic nucleotide- and NAD+-dependent effector-activation, and prevention of superinfection during pseudolysogeny. We reconstruct the RNA-repair systems of jumbo phages that counter the consequences of RNA-targeting host effectors. These findings also suggest that several jumbo phage proteins provide a snapshot of the systems found in ancient replicons preceding the last universal ancestor of cellular life.
Highlights
Viral genomes span a wide size-continuum, which at the lower end includes some of the smallest natural replicons and at the higher end exceeds that of several cellular genomes
The above-proposed cutoff based on the size distribution helps more objectively define the genomic size category that includes the jumbo phages and is treated as the focus of our analysis
We extend the previous observations of DNA N6 adenine methylases (DAMs) and DNA 5-cytosine methylases (DCMs) in jumbo phages to define several previously unrecognized exemplars of these [137] (Figure 5b)
Summary
Viral genomes span a wide size-continuum, which at the lower end includes some of the smallest natural replicons and at the higher end exceeds that of several cellular genomes. Most giant viruses are unified within the diverse clade of nucleocytoplasmic large DNA viruses (NCLDVs), which includes the poxviruses, iridoviruses and asfarviruses which infect animals and several large viruses that infect microbial eukaryotes [1,2,3]. It became clear early on that this virus is not just exemplary in virion size and in terms of its genome [6]. This was followed by the discovery of several giant phages infecting a diverse array of bacteria. In the past two decades, these giant phages entered the “genomic era” as their genomes were completely sequenced, revealing numerous remarkable aspects of their biology [7,8,9]
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