The Global Virome in One Network (VIRION): an Atlas of Vertebrate-Virus Associations

Abstract

Data that catalogue viral diversity on Earth have been fragmented across sources, disciplines, formats, and various degrees of open sharing, posing challenges for research on macroecology, evolution, and public health. Here, we solve this problem by establishing a dynamically maintained database of vertebrate-virus associations, called The Global Virome in One Network (VIRION). The VIRION database has been assembled through both reconciliation of static data sets and integration of dynamically updated databases. These data sources are all harmonized against one taxonomic backbone, including metadata on host and virus taxonomic validity and higher classification; additional metadata on sampling methodology and evidence strength are also available in a harmonized format. In total, the VIRION database is the largest open-source, open-access database of its kind, with roughly half a million unique records that include 9,521 resolved virus "species" (of which 1,661 are ICTV ratified), 3,692 resolved vertebrate host species, and 23,147 unique interactions between taxonomically valid organisms. Together, these data cover roughly a quarter of mammal diversity, a 10th of bird diversity, and ∼6% of the estimated total diversity of vertebrates, and a much larger proportion of their virome than any previous database. We show how these data can be used to test hypotheses about microbiology, ecology, and evolution and make suggestions for best practices that address the unique mix of evidence that coexists in these data. IMPORTANCE Animals and their viruses are connected by a sprawling, tangled network of species interactions. Data on the host-virus network are available from several sources, which use different naming conventions and often report metadata in different levels of detail. VIRION is a new database that combines several of these existing data sources, reconciles taxonomy to a single consistent backbone, and reports metadata in a format designed by and for virologists. Researchers can use VIRION to easily answer questions like "Can any fish viruses infect humans?" or "Which bats host coronaviruses?" or to build more advanced predictive models, making it an unprecedented step toward a full inventory of the global virome.

Keywords: data synthesis; ecological networks; global virome; host-virus interactions.

FIG 1

The VIRION pipeline. Data are integrated from a total of seven sources into one master file and a set of six disaggregated files that constitute the VIRION database. Data sources marked with a delta can be dynamically updated as new data are submitted to the source databases.

FIG 2

Comparative scope of data. Networks show all unique NCBI-recognized host-virus species pairs (viruses are red, hosts are blue) in the Host-Pathogen Phylogeny Project database (HP3, published in 2017) and VIRION. The information stored in VIRION is more extensive (including all vertebrates, not just mammals) but also far more information dense, describing a network with many more nodes and many more connections.

FIG 3

Taxonomic coverage across hosts. Each tree tip represents one host family, with the total number of viruses recorded in VIRION, the number that are NCBI resolved, and the number that are ICTV ratified. Note that the color scale varies across panels.

FIG 4

The geographic distribution of hosts and host-virus associations based on IUCN geographic range maps. Species are matched to the IUCN database using verbatim Latin names, without any manual correction. This is largely congruent for mammals (91.1%) and birds (93%) but less so for reptiles/amphibians (79%) and fish (47.6%), in part because some species may not yet be mapped. Particularly when working with the latter groups, users will likely need to manually cross-reference species names from the VIRION database to other sources.