Phage diversity, genomics and phylogeny

Abstract

Recent advances in viral metagenomics have enabled the rapid discovery of an unprecedented catalogue of phages in numerous environments, from the human gut to the deep ocean. Although these advances have expanded our understanding of phage genomic diversity, they also revealed that we have only scratched the surface in the discovery of novel viruses. Yet, despite the remarkable diversity of phages at the nucleotide sequence level, the structural proteins that form viral particles show strong similarities and conservation. Phages are uniquely interconnected from an evolutionary perspective and undergo multiple events of genetic exchange in response to the selective pressure of their hosts, which drives their diversity. In this Review, we explore phage diversity at the structural, genomic and community levels as well as the complex evolutionary relationships between phages, moulded by the mosaicity of their genomes.

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Fig. 1: Phage classification based on morphology and genome type.
Fig. 2: Number of complete genomes and genome size distribution in phage families.
Fig. 3: Integrating metagenomics, single-virus genomics, culture and microscopy to uncover viral diversity.
Fig. 4: Phage distribution and abundance in three ecosystems.
Fig. 5: Network representation of phage phylogeny.

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Acknowledgements

This work is supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Program and the Canadian Institutes of Health Research (team grant on Intestinal Microbiomics, Institute of Nutrition, Metabolism and Diabetes). M.B.D. is a recipient of graduate scholarships from the Fonds de Recherche du Québec — Nature et Technologies (FRQNT) as well as Sentinelle Nord, and is a recipient of the Goran-Enhorning Graduate Student Research Award from the Canadian Allergy, Asthma and Immunology Foundation. F.O. is a recipient of a fellowship from the Swiss National Science Foundation (Early Postdoc.Mobility). S.M. holds the Tier 1 Canada Research Chair in Bacteriophages and is a member of the PROTEO and Op+Lait FRQNT Networks.

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Glossary

Lysogens

Bacterial cells containing an integrated prophage, which can be induced, excised from the chromosome and enter the lytic cycle.

Mosaicism

The observation that different regions (genes and gene blocks) of the phage genomes have distinct evolutionary histories, owing to horizontal gene transfer events.

Viral metagenomics

Sequencing genomes of the viral fraction in a sample.

Polyhedral

A shape of the phage capsid, which consists of many polygonal faces and is most commonly found as an icosahedron (polyhedron with 20 faces).

Pleomorphic

Variability in shapes and sizes for phages.

HK97 fold

A 3D conformation termed after the capsid protein structure of phage HK97.

Portal complex

A dodecamer forming a central channel involved in viral DNA packaging and injection, providing a docking site for attachment of the tail machinery.

Synteny

Physical co-localization in the genome of genes with associated functions.

Microdiversity

Intra-population genetic variation.

Viral tagging metagenomics

A high-throughput method to link a virus to its host, consisting of labelling viruses with a fluorescent dye, collecting infected cells by flow cytometry and sequencing the viral DNA.

Lytic

A replication strategy where a phage takes control of the host cell to replicate its genetic material, produce its structural components, self-assemble to form new virions and burst (lyses) the cell to release new viral particles.

Virulent phages

Phages that can strictly undergo a lytic mode of replication.

Temperate phages

Phages that can perform either a lytic or a lysogenic mode of replication.

Cryptic

A non-functional prophage within a bacterial chromosome.

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Dion, M.B., Oechslin, F. & Moineau, S. Phage diversity, genomics and phylogeny. Nat Rev Microbiol 18, 125–138 (2020). https://doi.org/10.1038/s41579-019-0311-5

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