Taxonomy goes viral: a new set of consensus principles to classify the virosphere
The official body charged with virus classification has released four new principles that bring order to the viral world. This provides a unified framework that will enable all viruses to be classified, something vitally needed as genome technologies continue to discover millions of new virus species.
Since the ancient civilisations of Greece and Egypt, humans have attempted to classify life on Earth by putting organisms into related groups to understand life and infer relationships.
This classification of life, or taxonomy, took a giant step forward in the 18th century when Swedish botanist Carl Linnaeus established a hierarchical classification system that grouped organisms based on common characteristics. Significantly, he developed a Latin naming system that described each organism by group (genera) and specific name (species). Higher ranks brought related genera together into families, families into orders and so on through classes, phyla and kingdoms.
With publication of his ‘On the Origin of Species’ Charles Darwin gave us an understanding of how life forms on Earth evolve, and a framework on which organisms could be classified, or re-classified, based on evolutionary relationships. Based on Linnaeus’ template this evolutionary taxonomy has enabled construction of a tree of life on which every organism’s evolution can be traced back through more closely related organisms on the same branch, to common ancestors.
With advances in genome sequencing, we can now read the genetic code of any organism; ascertain how related organisms are to each other; and place them more accurately on ever more detailed taxonomic trees. This genomic taxonomy has been embraced by microbiologists, enabling them to classify microbes that had previously been impossible to distinguish on physical characteristics alone.
Genomic technology has also brought into focus just how much genetic diversity is out there; high throughput sequencing has shown there are millions of microbial species, rather more than the tens of thousands known and classified to date. The question of how taxonomy can include this huge unknown diversity of organisms that we cannot see, and sometimes cannot even culture, is starting to be addressed by official bodies comprised of different stakeholders.
The body mandated with developing and maintaining the taxonomy of viruses and their names is the International Committee on Taxonomy of Viruses (ICTV). In the pre-genomic age, viruses were classified by the shape of their particles, the type of nucleic acid in their genomes, or by other physical attributes such as the disease they caused or the organism they infected. But we now know from genomic sampling of various environments that there are millions of virus species, and they are associated with all domains of life.
In 2016, a consensus statement was published accepting the principle that viruses could be classified by their genome sequence, without the need for them to be cultured or their physical properties described (reference: Simmonds et al., 2016). Whilst this advance recognises the vast diversity that exists, it does not resolve ongoing debates about how viruses should be classified; should it be based on clinical significance, host, or other biological properties? Using Darwin’s principles viruses do not fit a universal evolutionary taxonomy as they appear to have evolved from a number of different, independent ancient evolutionary origins and have multiple trees of evolutionary history with little or no overlap.
To address this, the ICTV brought together an expert group of fundamental and clinical virologists, bioinformaticians and evolutionary and structural biologists to develop a community-led consensus on virus taxonomy. The outcomes of their discussions have now been published in the journal PLOS Biology and describe four central principles for establishing a universal virus taxonomy.
Overall, ICTV proposes that virus taxonomy can and should be based formally upon evolutionary relationships amongst viruses, with other physical properties used where appropriate to inform the placement of the ranks.
The first principle proposed is that viruses should be classified primarily based on the best attainable reconstruction of their evolutionary history. This currently recognises at least six virus groups, or realms, each of independent origin and sharing ‘hallmark’ genes; this reflects the way biologists construct trees of life right back to the earliest evolutionary origins of the cell.
The second principle recognises that other characteristics that naturally group viruses may be of use to researchers studying them, for example their host range or geographical spread. For official taxonomic classification, these properties can inform, but not override, evolutionary relatedness in the placement of viruses in the overall taxonomy.
The third principle recognises that there may be useful ways to group viruses that totally disregards evolutionary relationships. For example, the term arbovirus, derived from arthropod-born virus, is a useful classification in agriculture for viruses that are transmitted by insect vectors. However, this classification groups many viruses that are unrelated and, therefore, should not be called a virus taxonomy. In general, a universal evolutionary taxonomy doesn’t preclude alternative classifications that might be more appropriate for medical, veterinary or agricultural purposes.
These principles allow viruses to be classified seamlessly based on their genome sequence, and it is already allowing thousands more to be positioned on the different viral trees of life. We are in an age when it is possible to infer many of a virus’s attributes from its genome sequence, provided that sequence is complete and accurate. This guides the fourth principle which requires stringent quality control of genomic sequences to ensure they are suitable for use in taxonomic assignment.
These principles will help overcome decades of disagreement over virus classification, whilst at the same time harnessing the genomics revolution to provide a viral taxonomy that truly reflects and incorporates the vast diversity in the viral world.
Dr Evelien Adriaenssens from the Quadram Institute said: “It was an honour to lead and moderate the discussions on such an important topic as the future of virus taxonomy, with such a wonderful and distinguished set of virologists. The consensus we reached and the principles we established in this paper will give us the framework to include the – sometimes exasperating – diversity of viruses that has been discovered through sequence-based studies together with the viruses that we’ve known and loved for years.”
Prof. Peter Simmonds from the University of Oxford said: “It was a wonderful experience to share a workshop with world experts on virus diversity, genomics and classification. In the end, through collective efforts at the meeting and during an intensive writing up period, we made some major steps towards understanding each other’s’ points of view, creating consensus and developing a coherent set of principles that will hopefully guide the wider virology community. These principles traverse the range of seemingly intractable points of disagreement and contention that have bedevilled virus classification since its inception in the 1960s. Resolution of these conflicts provides a clear strategy for harnessing the genomics revolution in virology.”
Prof. Murilo Zerbini from the Universidade Federal de Viçosa, Brazil said: “Virus taxonomy has been transformed (for the best) by the deluge of metagenomics data, and we can now fill in many of the gaps that existed in our knowledge of the evolutionary relationships among viruses. The participants of the workshop agreed (after some intense debates!) that the incorporation of these data into the taxonomic framework allow the unification of virus taxonomy based on the four principles laid out in the paper. A clear view of the astounding diversity of the virosphere is finally within reach.”
Reference: Simmonds P, Adriaenssens EM, Zerbini FM, Abrescia NGA, Aiewsakun P, Alfenas-Zerbini P, et al. (2023) Four principles to establish a universal virus taxonomy. PLOS Biology 21(2): e3001922. 10.1371/journal.pbio.3001922 will be published at 11 AM Pacific Time / 2 PM Eastern Time / 7 PM British on Monday 13th February 2023