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Evidence for an Ancestral Association of Human Coronavirus 229E with Bats.
J Virol. 2015 Dec; 89(23):11858-70.JV

Abstract

We previously showed that close relatives of human coronavirus 229E (HCoV-229E) exist in African bats. The small sample and limited genomic characterizations have prevented further analyses so far. Here, we tested 2,087 fecal specimens from 11 bat species sampled in Ghana for HCoV-229E-related viruses by reverse transcription-PCR (RT-PCR). Only hipposiderid bats tested positive. To compare the genetic diversity of bat viruses and HCoV-229E, we tested historical isolates and diagnostic specimens sampled globally over 10 years. Bat viruses were 5- and 6-fold more diversified than HCoV-229E in the RNA-dependent RNA polymerase (RdRp) and spike genes. In phylogenetic analyses, HCoV-229E strains were monophyletic and not intermixed with animal viruses. Bat viruses formed three large clades in close and more distant sister relationships. A recently described 229E-related alpaca virus occupied an intermediate phylogenetic position between bat and human viruses. According to taxonomic criteria, human, alpaca, and bat viruses form a single CoV species showing evidence for multiple recombination events. HCoV-229E and the alpaca virus showed a major deletion in the spike S1 region compared to all bat viruses. Analyses of four full genomes from 229E-related bat CoVs revealed an eighth open reading frame (ORF8) located at the genomic 3' end. ORF8 also existed in the 229E-related alpaca virus. Reanalysis of HCoV-229E sequences showed a conserved transcription regulatory sequence preceding remnants of this ORF, suggesting its loss after acquisition of a 229E-related CoV by humans. These data suggested an evolutionary origin of 229E-related CoVs in hipposiderid bats, hypothetically with camelids as intermediate hosts preceding the establishment of HCoV-229E.

IMPORTANCE

The ancestral origins of major human coronaviruses (HCoVs) likely involve bat hosts. Here, we provide conclusive genetic evidence for an evolutionary origin of the common cold virus HCoV-229E in hipposiderid bats by analyzing a large sample of African bats and characterizing several bat viruses on a full-genome level. Our evolutionary analyses show that animal and human viruses are genetically closely related, can exchange genetic material, and form a single viral species. We show that the putative host switches leading to the formation of HCoV-229E were accompanied by major genomic changes, including deletions in the viral spike glycoprotein gene and loss of an open reading frame. We reanalyze a previously described genetically related alpaca virus and discuss the role of camelids as potential intermediate hosts between bat and human viruses. The evolutionary history of HCoV-229E likely shares important characteristics with that of the recently emerged highly pathogenic Middle East respiratory syndrome (MERS) coronavirus.

Authors+Show Affiliations

Institute of Virology, University of Bonn Medical Centre, Bonn, Germany German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn, Germany.Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia.Institute of Virology, University of Bonn Medical Centre, Bonn, Germany Laboratório de Virologia, Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo, Brazil.Institute of Virology, University of Bonn Medical Centre, Bonn, Germany Laboratório de Virologia, Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo, Brazil.Kumasi Centre for Collaborative Research in Tropical Medicine, Kumasi, Ghana.Kumasi Centre for Collaborative Research in Tropical Medicine, Kumasi, Ghana.Kumasi Centre for Collaborative Research in Tropical Medicine, Kumasi, Ghana.Centre International de Recherches Médicales de Franceville, Franceville, Gabon.Kwame Nkrumah University of Science and Technology, Kumasi, Ghana.Kwame Nkrumah University of Science and Technology, Kumasi, Ghana.Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic.Laboratório de Virologia, Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo, Brazil Instituto da Criança, Hospital das Clínicas da FMUSP, São Paulo, Brazil.Centre International de Recherches Médicales de Franceville, Franceville, Gabon Institut de Recherche pour le Développement, UMR 224 (MIVEGEC), IRD/CNRS/UM1, Montpellier, France.Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty Bern, University of Bern, Bern, Switzerland Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland.Department of Medical Microbiology, Academic Medical Center of the University of Amsterdam, Amsterdam, The Netherlands.School of Public Health, The University of Hong Kong, Hong Kong, Special Administrative Region, People's Republic of China.Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany Smithsonian Tropical Research Institute, Balboa, Panama.Institute of Virology, University of Bonn Medical Centre, Bonn, Germany German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn, Germany drosten@virology-bonn.de drexler@virology-bonn.de.Institute of Virology, University of Bonn Medical Centre, Bonn, Germany German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn, Germany drosten@virology-bonn.de drexler@virology-bonn.de.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

26378164

Citation

Corman, Victor Max, et al. "Evidence for an Ancestral Association of Human Coronavirus 229E With Bats." Journal of Virology, vol. 89, no. 23, 2015, pp. 11858-70.
Corman VM, Baldwin HJ, Tateno AF, et al. Evidence for an Ancestral Association of Human Coronavirus 229E with Bats. J Virol. 2015;89(23):11858-70.
Corman, V. M., Baldwin, H. J., Tateno, A. F., Zerbinati, R. M., Annan, A., Owusu, M., Nkrumah, E. E., Maganga, G. D., Oppong, S., Adu-Sarkodie, Y., Vallo, P., da Silva Filho, L. V., Leroy, E. M., Thiel, V., van der Hoek, L., Poon, L. L., Tschapka, M., Drosten, C., & Drexler, J. F. (2015). Evidence for an Ancestral Association of Human Coronavirus 229E with Bats. Journal of Virology, 89(23), 11858-70. https://doi.org/10.1128/JVI.01755-15
Corman VM, et al. Evidence for an Ancestral Association of Human Coronavirus 229E With Bats. J Virol. 2015;89(23):11858-70. PubMed PMID: 26378164.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Evidence for an Ancestral Association of Human Coronavirus 229E with Bats. AU - Corman,Victor Max, AU - Baldwin,Heather J, AU - Tateno,Adriana Fumie, AU - Zerbinati,Rodrigo Melim, AU - Annan,Augustina, AU - Owusu,Michael, AU - Nkrumah,Evans Ewald, AU - Maganga,Gael Darren, AU - Oppong,Samuel, AU - Adu-Sarkodie,Yaw, AU - Vallo,Peter, AU - da Silva Filho,Luiz Vicente Ribeiro Ferreira, AU - Leroy,Eric M, AU - Thiel,Volker, AU - van der Hoek,Lia, AU - Poon,Leo L M, AU - Tschapka,Marco, AU - Drosten,Christian, AU - Drexler,Jan Felix, Y1 - 2015/09/16/ PY - 2015/07/09/received PY - 2015/09/07/accepted PY - 2015/9/18/entrez PY - 2015/9/18/pubmed PY - 2016/3/2/medline SP - 11858 EP - 70 JF - Journal of virology JO - J Virol VL - 89 IS - 23 N2 - UNLABELLED: We previously showed that close relatives of human coronavirus 229E (HCoV-229E) exist in African bats. The small sample and limited genomic characterizations have prevented further analyses so far. Here, we tested 2,087 fecal specimens from 11 bat species sampled in Ghana for HCoV-229E-related viruses by reverse transcription-PCR (RT-PCR). Only hipposiderid bats tested positive. To compare the genetic diversity of bat viruses and HCoV-229E, we tested historical isolates and diagnostic specimens sampled globally over 10 years. Bat viruses were 5- and 6-fold more diversified than HCoV-229E in the RNA-dependent RNA polymerase (RdRp) and spike genes. In phylogenetic analyses, HCoV-229E strains were monophyletic and not intermixed with animal viruses. Bat viruses formed three large clades in close and more distant sister relationships. A recently described 229E-related alpaca virus occupied an intermediate phylogenetic position between bat and human viruses. According to taxonomic criteria, human, alpaca, and bat viruses form a single CoV species showing evidence for multiple recombination events. HCoV-229E and the alpaca virus showed a major deletion in the spike S1 region compared to all bat viruses. Analyses of four full genomes from 229E-related bat CoVs revealed an eighth open reading frame (ORF8) located at the genomic 3' end. ORF8 also existed in the 229E-related alpaca virus. Reanalysis of HCoV-229E sequences showed a conserved transcription regulatory sequence preceding remnants of this ORF, suggesting its loss after acquisition of a 229E-related CoV by humans. These data suggested an evolutionary origin of 229E-related CoVs in hipposiderid bats, hypothetically with camelids as intermediate hosts preceding the establishment of HCoV-229E. IMPORTANCE: The ancestral origins of major human coronaviruses (HCoVs) likely involve bat hosts. Here, we provide conclusive genetic evidence for an evolutionary origin of the common cold virus HCoV-229E in hipposiderid bats by analyzing a large sample of African bats and characterizing several bat viruses on a full-genome level. Our evolutionary analyses show that animal and human viruses are genetically closely related, can exchange genetic material, and form a single viral species. We show that the putative host switches leading to the formation of HCoV-229E were accompanied by major genomic changes, including deletions in the viral spike glycoprotein gene and loss of an open reading frame. We reanalyze a previously described genetically related alpaca virus and discuss the role of camelids as potential intermediate hosts between bat and human viruses. The evolutionary history of HCoV-229E likely shares important characteristics with that of the recently emerged highly pathogenic Middle East respiratory syndrome (MERS) coronavirus. SN - 1098-5514 UR - https://www.unboundmedicine.com/medline/citation/26378164/Evidence_for_an_Ancestral_Association_of_Human_Coronavirus_229E_with_Bats_ L2 - http://jvi.asm.org/cgi/pmidlookup?view=long&pmid=26378164 DB - PRIME DP - Unbound Medicine ER -