The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2

The present outbreak of a coronavirus-associated acute respiratory disease called coronavirus disease 19 (COVID-19) is the third documented spillover of an animal coronavirus to humans in only two decades that has resulted in a major epidemic. The Coronaviridae Study Group (CSG) of the International Committee on Taxonomy of Viruses, which is responsible for developing the classification of viruses and taxon nomenclature of the family Coronaviridae, has assessed the placement of the human pathogen, tentatively named 2019-nCoV, within the Coronaviridae. Based on phylogeny, taxonomy and established practice, the CSG recognizes this virus as forming a sister clade to the prototype human and bat severe acute respiratory syndrome coronaviruses (SARS-CoVs) of the species Severe acute respiratory syndrome-related coronavirus, and designates it as SARS-CoV-2. In order to facilitate communication, the CSG proposes to use the following naming convention for individual isolates: SARS-CoV-2/host/location/isolate/date. While the full spectrum of clinical manifestations associated with SARS-CoV-2 infections in humans remains to be determined, the independent zoonotic transmission of SARS-CoV and SARS-CoV-2 highlights the need for studying viruses at the species level to complement research focused on individual pathogenic viruses of immediate significance. This will improve our understanding of virus–host interactions in an ever-changing environment and enhance our preparedness for future outbreaks.

Upon a viral outbreak, it is important to rapidly establish whether the outbreak is caused by a new or a previously known virus (Box 1), as this helps decide which approaches and actions are most appropriate to detect the causative agent, control its transmission and limit potential consequences of the epidemic. The assessment of virus novelty also has implications for virus naming and, on a different timescale, helps to define research priorities in virology and public health.

For many human virus infections such as influenza virus1 or norovirus2 infections, well-established and internationally approved methods, standards and procedures are in place to identify and name the causative agents of these infections and report this information promptly to public health authorities and the general public. In outbreaks involving newly emerged viruses, the situation may be different, and appropriate procedures to deal with these viruses need to be established or refined with high priority.

Here, we present an assessment of the genetic relatedness of the newly identified human coronavirus3, provisionally named 2019-nCoV, to known coronaviruses, and detail the basis for (re)naming this virus severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which will be used hereafter. Given the public interest in naming newly emerging viruses and the diseases caused by these viruses in humans, we will give a brief introduction to virus discovery and classification — specifically the virus species concept — and the roles of different bodies, such as the World Health Organization (WHO) and the International Committee on Taxonomy of Viruses (ICTV), in this process. We hope this will help readers to better understand the scientific approach we have taken to arrive at this name, and we will also discuss implications of this analysis and naming decision.

Classifying and naming viruses and virus species

Defining the novelty of viruses is one of the topics that virus classification deals with. The classification of RNA viruses needs to consider their inherent genetic variability, which often results in two or more viruses with non-identical but similar genome sequences being regarded as variants of the same virus. This immediately poses the question of how much difference to an existing group is large enough to recognize the candidate virus as a member of a new, distinct group. This question is answered in best practice by evaluating the degree of relatedness of the candidate virus to previously identified viruses infecting the same host or established monophyletic groups of viruses, often known as genotypes or clades, which may or may not include viruses of different hosts. This is formally addressed in the framework of the official classification of virus taxonomy and is overseen and coordinated by the ICTV4. Viruses are clustered in taxa in a hierarchical scheme of ranks in which the species represents the lowest and most populous rank containing the least diverged groups (taxa) of viruses (Box 2). The ICTV maintains a Study Group for each virus family. The Study Groups are responsible for assigning viruses to virus species and taxa of higher ranks, such as subgenera, genera and subfamilies. In this context they play an important role in advancing the virus species concept and highlighting its significance5.

Virus nomenclature is a formal system of names used to label viruses and taxa. The fact that there are names for nearly all viruses within a species is due to the historical perception of viruses as causative agents of specific diseases in specific hosts, and to the way we usually catalogue and classify newly discovered viruses, which increasingly includes viruses that have not been linked to any known disease in their respective hosts (Box 1). The WHO, an agency of the United Nations, coordinates international public health activities aimed at combating, containing and mitigating the consequences of communicable diseases—including major virus epidemics—and is responsible for naming disease(s) caused by newly emerging human viruses. In doing so, the WHO often takes the traditional approach of linking names of specific diseases to viruses (Box 1) and assessing virus novelty by an apparent failure to detect the causative agent using established diagnostic assays.

Apart from disease, geography and the organism from which a given virus was isolated also dominate the nomenclature, occasionally engraving connections that may be accidental (rather than typical) or even stigmatizing, which should be avoided. Establishing a universal nomenclature for viruses was one of the major tasks of the ICTV when it was founded more than 50 years ago4. When the species rank was established in the taxonomy of viruses6, ICTV’s responsibility for naming viruses was shifted to naming and establishing species. ICTV Study Groups may also be involved in virus naming on a case-by-case basis as an extension of their official remit, as well as using the special expertise of their members. As virus species names are often very similar to the name of the founding member of the respective species, they are frequently confused in the literature with names of individual viruses in this species. The species name is italicized, starts with a capital letter and should not be spelled in an abbreviated form7; hence the species name Severe acute respiratory syndrome-related coronavirus. In contrast, this convention does not apply to virus names, hence severe acute respiratory syndrome coronavirus, or SARS-CoV, as it is widely known.

Defining the place of SARS-CoV-2 within the Coronaviridae

Researchers studying coronaviruses—a family of enveloped positive-strand RNA viruses infecting vertebrates8—have been confronted several times with the need to define whether a newly emerged virus causing a severe or even life-threatening disease in humans belongs to an existing or a new (yet-to-be-established) species. This happened with SARS9,10,11,12 and with Middle East respiratory syndrome (MERS)13,14 a few years later. Each time, the virus was placed in the taxonomy using information derived from a sequence-based family classification15,16.

The current classification of coronaviruses recognizes 39 species in 27 subgenera, five genera and two subfamilies that belong to the family Coronaviridae, suborder Cornidovirineae, order Nidovirales and realm Riboviria17,18,19 (Fig. 1). The family classification and taxonomy are developed by the Coronaviridae Study Group (CSG), a working group of the ICTV20. The CSG is responsible for assessing the place of new viruses through their relation to known viruses in established taxa, including placements relating to the species Severe acute respiratorysyndrome-related coronavirus. In the classification of nidoviruses, species are considered biological entities demarcated by a genetics-based method21, while generally virus species are perceived as man-made constructs22. To appreciate the difference between a nidoviral species and the viruses grouped therein, it may be instructive to look at their relationship in the context of the full taxonomy structure of several coronaviruses. Although these viruses were isolated at different times and locations from different human and animal hosts (with and without causing clinical disease), they all belong to the species Severe acute respiratorysyndrome-related coronavirus, and their relationship parallels that between human individuals and the species Homo sapiens (Fig. 1).

Fig. 1: Taxonomy of selected coronaviruses.
figure1

Shown is the full taxonomy of selected coronaviruses in comparison with the taxonomy of humans (the founders of virology and other eminent scientists represent individual human beings for the sake of this comparison), which is given only for categories (ranks) that are shared with the virus taxonomy. Note that these two taxonomies were independently developed using completely different criteria. Although no equivalence is implied, the species of coronaviruses is interpreted sensu stricto as accepted for the species of humans.

Even without knowing anything about the species concept, every human recognizes another human as a member of the same species. However, for assigning individual living organisms to most other species, specialized knowledge and tools for assessing inter-individual differences are required. The CSG uses a computational framework of comparative genomics23, which is shared by several ICTV Study Groups responsible for the classification and nomenclature of the order Nidovirales and coordinated by the ICTV Nidovirales Study Group (NSG)24 (Box 3). The Study Groups quantify and partition the variation in the most conserved replicative proteins encoded in open reading frames 1a and 1b (ORF1a/1b) of the coronavirus genome (Fig. 2a) to identify thresholds on pair-wise patristic distances (PPDs) that demarcate virus clusters at different ranks.

Fig. 2: Phylogeny of coronaviruses.
figure2

a, Concatenated multiple sequence alignments (MSAs) of the protein domain combination44 used for phylogenetic and DEmARC analyses of the family Coronaviridae. Shown are the locations of the replicative domains conserved in the ordert Nidovirales in relation to several other ORF1a/b-encoded domains and other major ORFs in the SARS-CoV genome. 5d, 5 domains: nsp5A-3CLpro, two beta-barrel domains of the 3C-like protease; nsp12-NiRAN, nidovirus RdRp-associated nucleotidyltransferase; nsp12-RdRp, RNA-dependent RNA polymerase; nsp13-HEL1 core, superfamily 1 helicase with upstream Zn-binding domain (nsp13-ZBD); nt, nucleotide. b, The maximum-likelihood tree of SARS-CoV was reconstructed by IQ‑TREE v.1.6.1 (ref. 45) using 83 sequences with the best fitting evolutionary model. Subsequently, the tree was purged from the most similar sequences and midpoint-rooted. Branch support was estimated using the Shimodaira–Hasegawa (SH)-like approximate likelihood ratio test with 1,000 replicates. GenBank IDs for all viruses except four are shown; SARS-CoV, AY274119.3; SARS-CoV-2, MN908947.3; SARSr-CoV_BtKY72, KY352407.1; SARS-CoV_PC4-227, AY613950.1. c, Shown is an IQ‑TREE maximum-likelihood tree of single virus representatives of thirteen species and five representatives of the species Severe acute respiratory syndrome-related coronavirus of the genus Betacoronavirus. The tree is rooted with HCoV-NL63 and HCoV-229E, representing two species of the genus Alphacoronavirus. Purple text highlights zoonotic viruses with varying pathogenicity in humans; orange text highlights common respiratory viruses that circulate in humans. Asterisks indicate two coronavirus species whose demarcations and names are pending approval from the ICTV and, thus, these names are not italicized.

Consistent with previous reports, SARS-CoV-2 clusters with SARS-CoVs in trees of the species Severe acute respiratory syndrome-related coronavirus (Fig. 2b) and the genus Betacoronavirus (Fig. 2c)25,26,27. Distance estimates between SARS-CoV-2 and the most closely related coronaviruses vary among different studies depending on the choice of measure (nucleotide or amino acid) and genome region. Accordingly, there is no agreement yet on the exact taxonomic position of SARS-CoV-2 within the subgenus Sarbecovirus. When we included SARS-CoV-2 in the dataset used for the most recent update (May 2019) of the coronavirus taxonomy currently being considered by ICTV19, which includes 2,505 coronaviruses, the species composition was not affected and the virus was assigned to the species Severe acute respiratory syndrome-related coronavirus, as detailed in Box 4.

With respect to novelty, SARS-CoV-2 differs from the two other zoonotic coronaviruses, SARS-CoV and MERS-CoV, introduced to humans earlier in the twenty-first century. Previously, the CSG established that each of these two viruses prototype a new species in a new informal subgroup of the genus Betacoronavirus15,16. These two informal subgroups were recently recognized as subgenera Sarbecovirus and Merbecovirus18,28,29 when the subgenus rank was established in the virus taxonomy30. Being the first identified representatives of a new species, unique names were introduced for the two viruses and their taxa in line with the common practice and state of virus taxonomy at the respective times of isolation. The situation with SARS-CoV-2 is fundamentally different because this virus is assigned to an existing species that contains hundreds of known viruses predominantly isolated from humans and diverse bats. All these viruses have names derived from SARS-CoV, although only the human isolates collected during the 2002–2003 outbreak have been confirmed to cause SARS in infected individuals. Thus, the reference to SARS in all these virus names (combined with the use of specific prefixes, suffixes and/or genome sequence IDs in public databases) acknowledges the phylogenetic (rather than clinical disease-based) grouping of the respective virus with the prototypic virus in that species (SARS-CoV). The CSG chose the name SARS-CoV-2 based on the established practice for naming viruses in this species and the relatively distant relationship of this virus to the prototype SARS-CoV in a species tree and the distance space (Fig. 2b and the figure in Box 4).

The available yet limited epidemiological and clinical data for SARS-CoV-2 suggest that the disease spectrum and transmission efficiency of this virus31,32,33,34,35 differ from those reported for SARS-CoV9. To accommodate the wide spectrum of clinical presentations and outcomes of infections caused by SARS-CoV-2 (ranging from asymptomatic to severe or even fatal in some cases)31, the WHO recently introduced a rather unspecific name (coronavirus disease 19, also known as COVID-19 (ref. 36)) to denote this disease. Also, the diagnostic methods used to confirm SARS-CoV-2 infections are not identical to those of SARS-CoV. This is reflected by the specific recommendations for public health practitioners, healthcare workers and laboratory diagnostic staff for SARS-CoV-2 (for example, the WHO guidelines for SARS-CoV-2 (ref. 37). By uncoupling the naming conventions used for coronaviruses and the diseases that some of them cause in humans and animals, we wish to support the WHO in its efforts to establish disease names in the most appropriate way (for further information, see the WHO’s guidelines for disease naming38). The further advancement of naming conventions is also important because the ongoing discovery of new human and animal viruses by next-generation sequencing technologies can be expected to produce an increasing number of viruses that do not (easily) fit the virus–disease model that was widely used in the pre-genomic era (Box 1). Having now established different names for the causative virus (SARS-CoV-2) and the disease (COVID-19), the CSG hopes that this will raise awareness in both the general public and public health authorities regarding the difference between these two entities. The CSG promotes this clear distinction because it will help improve the outbreak management and also reduces the risk of confusing virus and disease, as has been the case over many years with SARS-CoV (the virus) and SARS (the disease).

To facilitate good practice and scientific exchange, the CSG recommends that researchers describing new viruses (that is, isolates) in this species adopt a standardized format for public databases and publications that closely resembles the formats used for isolates of avian coronaviruses39, filoviruses40 and influenza virus1. The proposed naming convention includes a reference to the host organism that the virus was isolated from, the place of isolation (geographic location), an isolate or strain number, and the time of isolation (year or more detailed) in the format virus/host/location/isolate/date; for example, SARS-CoV-2/human/Wuhan/X1/2019. This complete designation along with additional and important characteristics, such as pathogenic potential in humans or other hosts, should be included in the submission of each isolate genome sequence to public databases such as GenBank. In publications, this name could be further extended with a sequence database ID—for example, SARS-CoV-2/human/Wuhan/X1/2019_XYZ12345 (fictional example)—when first mentioned in the text. We believe that this format will provide critical metadata on the major characteristics of each particular virus isolate (genome sequence) required for subsequent epidemiological and other studies, as well as for control measures.

Expanding the focus from pathogens to virus species

Historically, public health and fundamental research have been focused on the detection, containment, treatment and analysis of viruses that are pathogenic to humans following their discovery (a reactive approach). Exploring and defining their biological characteristics in the context of the entire natural diversity as a species has never been a priority. The emergence of SARS-CoV-2 as a human pathogen in December 2019 may thus be perceived as completely independent from the SARS-CoV outbreak in 2002–2003. Although SARS-CoV-2 is indeed not a descendent of SARS-CoV (Fig. 2b), and the introduction of each of these viruses into humans was likely facilitated by independent unknown external factors, the two viruses are genetically so close to each other (Fig. 2c, panel c of the figure in Box 4) that their evolutionary histories and characteristics are mutually informative.

The currently known viruses of the species Severe acute respiratory syndrome-related coronavirus may be as (poorly) representative for this particular species as the few individuals that we selected to represent H. sapiens in Fig. 1. It is thus reasonable to assume that this biased knowledge of the natural diversity of the species Severe acute respiratory syndrome-related coronavirus limits our current understanding of fundamental aspects of the biology of this species and, as a consequence, our abilities to control zoonotic spillovers to humans. Future studies aimed at understanding the ecology of these viruses and advancing the accuracy and resolution of evolutionary analyses41 would benefit greatly from adjusting our research and sampling strategies. This needs to include an expansion of our current research focus on human pathogens and their adaptation to specific hosts to other viruses in this species. To illustrate the great potential of species-wide studies, it may again be instructive to draw a parallel to H. sapiens, and specifically to the impressive advancements in personalized medicine in recent years. Results of extensive genetic analyses of large numbers of individuals representing diverse populations from all continents have been translated into clinical applications and greatly contribute to optimizing patient-specific diagnostics and therapy. They were instrumental in identifying reliable predictive markers for specific diseases as well as genomic sites that are under selection. It thus seems reasonable to expect that genome-based analyses with a comparable species coverage will be similarly insightful for coronaviruses. Also, additional diagnostic tools that target the entire species should be developed to complement existing tools optimized to detect individual pathogenic variants (a proactive approach). Technical solutions to this problem are already available; for example, in the context of multiplex PCR-based assays42. The costs for developing and applying (combined or separate) species- and virus-specific diagnostic tests in specific clinical and/or epidemiological settings may help to better appreciate the biological diversity and zoonotic potential of specific virus species and their members. Also, the further reduction of time required to identify the causative agents of novel virus infections will contribute to limiting the enormous social and economic consequences of large outbreaks. To advance such studies, innovative fundraising approaches may be required.

Although this Consensus Statement focuses on a single virus species, the issues raised apply to other species in the family and possibly beyond. A first step towards appreciation of this species and others would be for researchers, journals, databases and other relevant bodies to adopt proper referencing to the full taxonomy of coronaviruses under study, including explicit mentioning of the relevant virus species and the specific virus(es) within the species using the ICTV naming rules explained above. This naming convention is, regretfully, rarely observed in common practice, with mixing of virus and species names being frequently found in the literature (including by the authors of this Consensus Statement on several past occasions). The adoption of accurate virus-naming practices should be facilitated by the major revision of the virus species nomenclature that is currently being discussed by the ICTV and is being planned for implementation in the near future43. With this change in place, the CSG is resolved to address the existing significant overlap between virus and species names that complicates the appreciation and use of the species concept in its application to coronaviruses.

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Acknowledgements

Work on DEmARC advancement and coronavirus and nidovirus taxonomies was supported by the EU Horizon 2020 EVAg 653316 project and the LUMC MoBiLe program (to A.E.G.), and on coronavirus and nidovirus taxonomies by a Mercator Fellowship by the Deutsche Forschungsgemeinschaft (to A.E.G.) in the context of the SFB1021 (A01 to J.Z.).

We thank all researchers who released SARS-CoV-2 genome sequences through the GISAID initiative and particularly the authors of the GenBank MN908947 genome sequence: F. Wu, S. Zhao, B. Yu, Y. M. Chen, W. Wang, Z. G. Song, Y. Hu, Z. W. Tao, J. H. Tian, Y. Y. Pei, M. L. Yuan, Y. L. Zhang, F. H. Dai, Y. Liu, Q. M. Wang, J. J. Zheng, L. Xu, E. C. Holmes and Y. Z. Zhang. We thank S. G. Siddell, R. A. M. Fouchier, and J. H. Kuhn for their comments on a manuscript version posted on 11 February 2020 to bioRxiv. A.E.G. and J.Z. thank W. J. M. Spaan, A. J. Davison and E. J. Lefkowitz for support. A.E.G. thanks members of the ICTV ExecutiveCommittee for discussions of classification and nomenclature issues relevant to this paper.

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S.C.B., R.S.B., C.D., R.J.D.G., A.E.G., B.L.H., B.W.N., S.P., L.L.M.P., I.S. and J.Z. are members of the CSG, chaired by J.Z.; R. J.D.G., A.E.G., C.L., B.W.N. and J.Z. are members of the NSG, chaired by A.E.G.; A.E.G. and J.Z. are members of the ICTV. A.E.G., A.A.G., C.L., A.M.L., D.P., D.V.S. and I.A.S. are members of the DEmARC team led by A.E.G. D.V.S. generated the classification of SARS-CoV-2 using a computational pipeline developed by A.A.G. and using software developed by the DEmARC team; the CSG considered and approved this classification, and subsequently debated and decided on the virus name. A.E.G. and J.Z. wrote the manuscript. A.E.G. and D.V.S. generated the figures. All authors reviewed the manuscript and approved its submission for publication.

Correspondence to Alexander E. Gorbalenya or John Ziebuhr.

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Gorbalenya, A.E., Baker, S.C., Baric, R.S. et al. The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol 5, 536–544 (2020). https://doi.org/10.1038/s41564-020-0695-z

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