Improving Virus Taxonomy by Recontextualizing Sequence-Based Classification with Biologically Relevant Data: the Case of the Alphacoronavirus 1 Species.

Jean Kaoru Millet,Gary R. Whittaker,Nicole M. André

doi:10.1128/mspheredirect.00463-17

Jean Kaoru Millet, Gary R. Whittaker

Open Access

https://doi.org/10.1128/mspheredirect.00463-17

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Abstract

The difficulties related to virus taxonomy have been amplified by recent advances in next-generation sequencing and metagenomics, prompting the field to revisit the question of what constitutes a useful viral classification. Here, taking a challenging classification found in coronaviruses, we argue that consideration of biological properties in addition to sequence-based demarcations is critical for generating useful taxonomy that recapitulates complex evolutionary histories. Within the Alphacoronavirus genus, the Alphacoronavirus 1 species encompasses several biologically distinct viruses. We carried out functionally based phylogenetic analysis, centered on the spike gene, which encodes the main surface antigen and primary driver of tropism and pathogenesis. Within the Alphacoronavirus 1 species, we identify clade A (encompassing serotype I feline coronavirus [FCoV] and canine coronavirus [CCoV]) and clade B (grouping serotype II FCoV and CCoV and transmissible gastroenteritis virus [TGEV]-like viruses). We propose this clade designation, along with the newly proposed Alphacoronavirus 2 species, as an improved way to classify the Alphacoronavirus genus. IMPORTANCE Our work focuses on improving the classification of the Alphacoronavirus genus. The Alphacoronavirus 1 species groups viruses of veterinary importance that infect distinct mammalian hosts and includes canine and feline coronaviruses and transmissible gastroenteritis virus. It is the prototype species of the Alphacoronavirus genus; however, it encompasses biologically distinct viruses. To better characterize this prototypical species, we performed phylogenetic analyses based on the sequences of the spike protein, one of the main determinants of tropism and pathogenesis, and reveal the existence of two subgroups or clades that fit with previously established serotype demarcations. We propose a new clade designation to better classify Alphacoronavirus 1 members.

Highlights

The difficulties related to virus taxonomy have been amplified by recent advances in next-generation sequencing and metagenomics, prompting the field to revisit the question of what constitutes a useful viral classification
Because of the critical role played by S protein in virus entry, pathogenesis, and tropism and since the S proteins of serotype I and II strains differ greatly, we propose a classification of Alphacoronavirus 1 strains into two clades (Alphacoronavirus 1 clades A and B), using a functionally based S protein sequence classification that reflects the previously determined serologically based demarcation
Analysis based on the ORF1ab polyprotein sequence reveals very similar phylogenetic relationships, with a partitioning of feline coronavirus (FCoV) strains in one subgroup and canine coronavirus (CCoV) and transmissible gastroenteritis virus (TGEV) strains in another (Fig. 1B)

Summary

Introduction

The difficulties related to virus taxonomy have been amplified by recent advances in next-generation sequencing and metagenomics, prompting the field to revisit the question of what constitutes a useful viral classification. The Alphacoronavirus 1 species groups viruses of veterinary importance that infect distinct mammalian hosts and includes canine and feline coronaviruses and transmissible gastroenteritis virus. It is the prototype species of the Alphacoronavirus genus; it encompasses biologically distinct viruses. We focus on the Alphacoronavirus 1 species of the Alphacoronavirus genus, to highlight some issues and limitations with current classification schemes and to provide some suggestions to improve them This type species groups strains infecting distinct hosts and is based on a threshold level of more than 90% sequence identity in key coronavirus (CoV) replicase domains (pp1ab polyprotein and ORF1ab gene). Coronaviruses (CoVs) are classified into four genera, with Alphacoronavirus and Betacoronavirus containing members that infect mostly mammalian species and Gammacoronavirus and Deltacoronavirus grouping viruses infecting both birds and mammals [4]

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