Towards a unifying phylogenomic framework for tailed phages
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Background
Classifying viruses systematically has remained a key challenge of virology due to the absence of universal genes and vast genetic diversity of viruses. In particular, the most dominant and diverse group of viruses, the tailed double-stranded DNA viruses of prokaryotes belonging to the class Caudoviricetes, lack sufficient homology in the genetic machinery that unifies them to reconstruct inclusive, stable phylogenies of these genes. While previous approaches to organize tailed phage diversity have managed to distinguish various taxonomic levels, these methods are limited in scalability and reproducibility, and they do not include modes of evolution, like gene gains and losses.
Results
Here, we present a novel, comprehensive and reproducible framework for examining evolutionary relationships of tailed phages. In this framework, we compare phage genomes based on presences and absences of a fixed set of gene families which is used as binary trait data that is input into maximum likelihood models, which include heterogeneous rates of trait losses and gains. Our resulting phylogeny stably recovers known taxonomic families of tailed phages, with and without the inclusion of metagenomic phages. We also quantify the mosaicism of replication and structural genes among known families. Our results suggest that these exchanges likely underpin the emergence of new families. Additionally, we apply this framework to large phages (>100 kilobases) to map emergences of traits associated with genome expansion.
Conclusion
Taken together, this evolutionary framework for charting and organizing tailed phage diversity improves the systemization of phage taxonomy, which can unify phage studies and advance our understanding of their evolution.
