Virosphere Belongs to Biosphere Say Virus Taxonomists

Researchers now have the opportunity to classify every virus as they do for any other biological entity: applying the computational tools of comparative genomics across the full scale of divergence and, in terms of ranks, with a resolution comparable to their hosts

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Virus; what comes to mind? Yesterday, it was a computer bug, HIV, and Ebola virus, probably in this order. Today, it is COVID-19 (which is actually a disease), coronavirus, and SARS-CoV-2, very likely in this order. We don’t know what will be in the spotlight tomorrow, and the turmoil that might ensue, but I hope that the widespread fear of viruses will be alleviated by studies of the virosphere and virus ecology, such as those regularly presented by colleagues in this blog. A recent Consensus Statement, which I will hereafter call the ART paper, may contribute to bringing that future an inch closer.

The ART paper, which was written by senior representatives of the International Committee on Taxonomy of Viruses (ICTV), the overseer of all matters of virus taxonomy, describes the introduction of a new rank structure of virus classification that was expanded to closely resemble a Linnean taxonomy, as used elsewhere in biology. To appreciate the scale of this development, which may be “revolutionary” to some, just look at a prevailing perception of virus diversity depicted at the otherwise fascinating Micropia Museum in Amsterdam (Figure 1): four small “virus” icons sitting next to each other in the left corner and next, to the right, a large Tree of Life (ToL) detailing evolutionary relationships of cellular life forms, from microbes to humans. While some may not agree with the accompanying text saying viruses are not life forms, few will challenge the depiction per se

Figure 1. Viruses and ToL at the Micropia Museum, Amsterdam. © Alexander Gorbalenya

It is correct that viruses have no place on the ToL, which itself is under increasing scrutiny, but researchers now have the opportunity to classify every virus - as any other biological entity - across the full scale of divergence and with a rank resolution rivalling or exceeding that used for their hosts. This development creates a stage for crosstalk between the taxonomies of viruses and cellular organisms within a common framework of evolutionary biology.

My road to this publication could be traced back some 45 years ago when I was introduced to virology in the laboratory of Vadim Agol in Moscow. Vadim approached viruses as curiosities of the molecular world, both as subjects of study and classification [1], which seemed pretty convincing until I learned later how far it was from the pathogen-centrist view that shaped virology. In the meantime, I had observed the birth of virus genomics and comparative genomics, which illuminated distant inter-virus relationships that did not fit easily into paradigm of rapidly evolving viruses and remained outside the scope of virus taxonomy until the advent of the new rank structure.

Fast forward to December 2019, when I received an email from Nonia Pariente, the then Editor-In-Chief of Nature Microbiology, informing me about their willingness to proceed, conditionally, with the publication of the ART paper. This good news came at the time when I visited John Ziebuhr, Chair of Coronaviridae Study Group (CSG), to continue our collaboration on the taxonomy of the family Coronaviridae, which includes SARS-CoV, and other related families that form together the order Nidovirales. By a sheer coincidence, it was that very project which prompted me in 2016 to initiate a discussion at a meeting of the ICTV Executive Committee (ICTV-EC) about the then limited rank structure of virus taxonomy. Moreover, the ART paper included a figure that detailed the distant relationship between SARS-CoV and Ebola virus (Figure 2) to reach out to people who are primarily interested in pathogenic viruses. Unexpectedly, the Ebola virus vs SARS-CoV comparison may now look particularly timely, thanks to the identification of a new coronavirus during the same December 2019. Using the advanced taxonomy rank structure, the CSG classified that virus as a sibling of SARS-CoV and named it SARS-CoV-2 [2].

Figure 2. Classification of three viruses in the 15-rank taxonomic hierarchy

There are no experiments or field observations reported in the ART paper, just an overview of discussions about conceptual and practical matters such as nomenclature issues. Yet it took almost four years from inception to publication, not counting all the years of hoping that this moment would arrive one day. This is testament to how complex and divisive the topic has been. From one hand, the new rank structure has already been used to present a vision of the ordered virosphere [3]. At the same time, I am aware of voices wary of the burden of filling the new ranks and sceptical about the benefits of such an exercise. Notwithstanding this criticism, the reported advance reflects a sea change that was brought about by many colleagues including co-authors of the ART paper, who represent different sections of virology and many countries. They are six colleagues (Stuart Siddell, Mart Krupovic, Arcady Mushegian, Andrew Kropinski, Arvind Varsani, and Jens Kuhn) who were involved in the detailed discussion of the ART proposal (Figure 3), plus fifteen other ICTV-EC members who considered the project on many occasions (Mike Adams, Andrew Davison, Bas Dutilh, Balazs Harrach, Bob Harrison, Sandra Junglen, Andrew King, Nick Knowles, Elliot Lefkowitz, Max Nibert, Luisa Rubino, Sead Sabanadzovic, Helene Sanfacon, Peter Simmonds, Peter Walker, and Murilo Zerbini). Each word of the ART paper is the result of many revisions. I wish you happy reading!

Figure 3. The Additional Ranks in Taxonomy Fellows (from left to right): Stuart Siddell, Mart Krupovic, Jens Kuhn, Andrew Kropinski, Arvind Varsani, Arcady Mushegian, Alexander Gorbalenya; after ICTV-EC approved conditionally the ART proposal, Singapore, July 16, 2017.    © Helene Sanfacon

PS: If you like viruses, computing and sense of order, you are looking for a new or first start of an independent line of research, and want to learn how good you are, consider the challenge of establishing a teaching curriculum on virus taxonomy and acquire funding to develop a brand-new taxonomy of viruses in the era of grand exploration of virosphere.

  1. Agol, V.I., In pursuit of intriguing puzzles. Virology, 2020. 539: p. 49-60.
  2. Gorbalenya, A.E., et al., The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nature Microbiology, 2020. 5(4): p. 536-544.
  3. Koonin, E.V., et al., Global Organization and Proposed Megataxonomy of the Virus World. Microbiol Mol Biol Rev, 2020. 84(2).

 

Go to the profile of Alexander E. Gorbalenya

Alexander E. Gorbalenya

Professor Emeritus, Leiden University Medical Center

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