Bacteriophage genome size evolution is understudied, with conflicting hypotheses about whether genomes gain or lose DNA content over time. We here attempt to address this conflict using in silico methods to build a phylogeny of Arthrobacter viruses whose genome sizes are known. Amino acid sequences of three, widely-occurring genes (holin, terminase, portal protein) were collected from 53 Arthrobacter phages (from 16 clusters) and four outgroup viruses (two clusters) using common bioinformatics approaches. Genome sizes amongst these viruses span from ~15kb to ~175kb and were gap-coded into nine categories to ignore most small size shifts. Phylogenetic analysis of the aligned, concatenated sequences (2,639 aa) resulted in three, most-parsimonious trees of length 12,726. All phage clusters (and subclusters) were recovered as monophyletic in these trees but there was some variation within clusters among them. While cluster membership is highly predictive of genome size, the relationships among clusters revealed a complex, size change pattern—Genome size increased seven times and decreased five times in the ingroup. Our topology also suggests that ingroup taxa lost the portal protein gene twice and the holin gene at least four times, but these losses themselves do not explain reconstructed genome size changes. Our results therefore demonstrate a complexity and heterogeneity to viral genome dynamics and document the absence of a consistent pattern of genome size evolution in Arthrobacter bacteriophages, contrary to the prevailing, unimodal hypotheses for viral genome evolution.

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