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Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences.

Jan Felix Drexler1 Florian Gloza-Rausch Jörg Glende Victor Max Corman Doreen Muth Matthias Goettsche Antje Seebens Matthias Niedrig Susanne Pfefferle Stoian Yordanov Lyubomir Zhelyazkov Uwe Hermanns Peter Vallo Alexander Lukashev Marcel Alexander Müller Hongkui Deng Georg Herrler Christian Drosten
Affiliations 1 institutions
  1. Institute of Virology, University of Bonn Medical Centre, 53127 Bonn, Germany.
PMID 20686038 2010 J Virol eng ppublish
PubMed DOI Browse context

Article

Publication summary

Bats may host emerging viruses, including coronaviruses (CoV). We conducted an evaluation of CoV in rhinolophid and vespertilionid bat species common in Europe. Rhinolophids carried severe acute respiratory syndrome (SARS)-related CoV at high frequencies and concentrations (26% of animals are positive; up to 2.4×10(8) copies per gram of feces), as well as two Alphacoronavirus clades, one novel and one related to the HKU2 clade. All three clades present in Miniopterus bats in China (HKU7, HKU8, and 1A related) were also present in European Miniopterus bats. An additional novel Alphacoronavirus clade (bat CoV [BtCoV]/BNM98-30) was detected in Nyctalus leisleri. A CoV grouping criterion was developed by comparing amino acid identities across an 816-bp fragment of the RNA-dependent RNA polymerases (RdRp) of all accepted mammalian CoV species (RdRp-based grouping units [RGU]). Criteria for defining separate RGU in mammalian CoV were a >4.8% amino acid distance for alphacoronaviruses and a >6.3% distance for betacoronaviruses. All the above-mentioned novel clades represented independent RGU. Strict associations between CoV RGU and host bat genera were confirmed for six independent RGU represented simultaneously in China and Europe. A SARS-related virus (BtCoV/BM48-31/Bulgaria/2008) from a Rhinolophus blasii (Rhi bla) bat was fully sequenced. It is predicted that proteins 3b and 6 were highly divergent from those proteins in all known SARS-related CoV. Open reading frame 8 (ORF8) was surprisingly absent. Surface expression of spike and staining with sera of SARS survivors suggested low antigenic overlap with SARS CoV. However, the receptor binding domain of SARS CoV showed higher similarity with that of BtCoV/BM48-31/Bulgaria/2008 than with that of any Chinese bat-borne CoV. Critical spike domains 472 and 487 were identical and similar, respectively. This study underlines the importance of assessments of the zoonotic potential of widely distributed bat-borne CoV.

Animals Base Sequence China Chiroptera Coronavirus Europe Genome, Viral Humans RNA-Dependent RNA Polymerase Severe acute respiratory syndrome-related coronavirus

Structured evidence records

Evidence records

8 total
Zoonotic Surveillance 4 records
Zoonotic Surveillance Extraction confidence 0.95
Key finding

Genomic surveillance identified SARS-related coronaviruses in European rhinolophid bats with high prevalence and viral loads.

Virus
SARSr-CoV
Location
Europe
Supporting text

We conducted an evaluation of CoV in rhinolophid and vespertilionid bat species common in Europe. Rhinolophids carried severe acute respiratory syndrome (SARS)-related CoV at high frequencies and concentrations (26% of animals are positive; up to 2.4×10(8) copies per gram of feces).

Method
genomic characterization
Sample type
feces
Geographic raw
Europe
Zoonotic Surveillance Extraction confidence 0.90
Key finding

A novel Alphacoronavirus clade was detected through surveillance in Nyctalus leisleri bats.

Location
Europe
Supporting text

An additional novel Alphacoronavirus clade (bat CoV [BtCoV]/BNM98-30) was detected in Nyctalus leisleri.

Method
genomic characterization
Geographic raw
Europe
Zoonotic Surveillance Extraction confidence 0.90
Key finding

Surveillance found HKU7, HKU8, and 1A-related coronaviruses in European Miniopterus bats corresponding to clades previously identified in China.

Location
Europe
Supporting text

All three clades present in Miniopterus bats in China (HKU7, HKU8, and 1A related) were also present in European Miniopterus bats.

Method
genomic characterization
Geographic raw
Europe
Zoonotic Surveillance Extraction confidence 0.90
Key finding

Full genomic sequencing identified a SARS-related coronavirus from a Rhinolophus blasii bat in Bulgaria.

Location
Bulgaria Bulgaria
Supporting text

A SARS-related virus (BtCoV/BM48-31/Bulgaria/2008) from a Rhinolophus blasii (Rhi bla) bat was fully sequenced.

Method
genomic sequencing
Geographic raw
Bulgaria
Country inferred
Bulgaria
Genomic Evolution 2 records
Genomic Evolution Extraction confidence 0.95
Key finding

Full genome sequencing of SARS-related coronavirus BtCoV/BM48-31/Bulgaria/2008 from a European Rhinolophus blasii bat revealed unique genomic features including absence of ORF8 and high divergence in proteins 3b and 6, indicating distinct evolutionary lineage closely related to SARS-CoV.

Location
Not specified
Supporting text

A SARS-related virus (BtCoV/BM48-31/Bulgaria/2008) from a Rhinolophus blasii bat was fully sequenced. It is predicted that proteins 3b and 6 were highly divergent from those proteins in all known SARS-related CoV. Open reading frame 8 (ORF8) was absent. The receptor binding domain of SARS CoV showed higher similarity with that of BtCoV/BM48-31/Bulgaria/2008 than with that of any Chinese bat-borne CoV.

Genes or proteins
3b; 6; ORF8; spike
Analysis methods
genome sequencing; comparative genomic analysis
Genomic Evolution Extraction confidence 0.90
Key finding

Comparative analysis of RdRp gene sequences from mammalian coronaviruses defined novel alphacoronavirus and betacoronavirus clades as independent RdRp-based grouping units, indicating significant evolutionary diversity among bat CoV.

Host
Chiroptera
Location
Not specified
Supporting text

A CoV grouping criterion was developed by comparing amino acid identities across an 816-bp fragment of the RNA-dependent RNA polymerases (RdRp) of all accepted mammalian CoV species (RdRp-based grouping units [RGU]). Criteria for defining separate RGU in mammalian CoV were set, and novel alphacoronavirus and betacoronavirus clades representing independent RGU were identified.

Genes or proteins
RNA-dependent RNA polymerase
Analysis methods
comparative genomic analysis; phylogenetic analysis
Molecular Adaptation 1 records
Molecular Adaptation Extraction confidence 0.80
Key finding

BtCoV/BM48-31/Bulgaria/2008 from a European Rhinolophus blasii bat shows molecular adaptation compared with SARS-CoV, including divergence in 3b and 6 proteins, loss of ORF8, and spike receptor-binding residues identical or similar to critical SARS-CoV positions 472 and 487, indicating potential receptor compatibility and antigenic differentiation.

Host
Not specified
Location
Not specified
Supporting text

A SARS-related virus (BtCoV/BM48-31/Bulgaria/2008) from a Rhinolophus blasii bat was fully sequenced. It is predicted that proteins 3b and 6 were highly divergent from those proteins in all known SARS-related CoV. Open reading frame 8 (ORF8) was surprisingly absent. Surface expression of spike and staining with sera of SARS survivors suggested low antigenic overlap with SARS CoV. However, the receptor binding domain of SARS CoV showed higher similarity with that of BtCoV/BM48-31/Bulgaria/2008 than with that of any Chinese bat-borne CoV. Critical spike domains 472 and 487 were identical and similar, respectively.

Genes or proteins
3b; 6; ORF8; spike
Mutations
spike position 472; spike position 487
Mechanism types
antigenic_variation; receptor_binding; host_adaptation
Receptor Usage 1 records
Receptor Usage Extraction confidence 0.70
Key finding

SARS-related bat coronavirus BtCoV/BM48-31/Bulgaria/2008 displayed receptor binding domain similarity to SARS-CoV, indicating possible receptor compatibility.

Location
Not specified
Supporting text

The receptor binding domain of SARS CoV showed higher similarity with that of BtCoV/BM48-31/Bulgaria/2008 than with that of any Chinese bat-borne CoV. Critical spike domains 472 and 487 were identical and similar, respectively.

Method
sequence comparison; antigenic analysis
Receptors
receptor binding domain