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Review
. 2014 Jan:101:45-56.
doi: 10.1016/j.antiviral.2013.10.013. Epub 2013 Oct 31.

Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS

Jan Felix Drexler  1 , Victor Max Corman  2 , Christian Drosten  2
Affiliations
Review

Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS

Jan Felix Drexler et al. Antiviral Res. 2014 Jan.

Abstract

In 2002/2003, a novel coronavirus (CoV) caused a pandemic, infecting more than 8000 people, of whom nearly 10% died. This virus, termed severe acute respiratory syndrome-CoV was linked to a zoonotic origin from rhinolophid bats in 2005. Since then, numerous studies have described novel bat CoVs, including close relatives of the newly emerging Middle East respiratory syndrome (MERS)-CoV. In this paper we discuss CoV genomic properties and compare different taxonomic approaches in light of the technical difficulties of obtaining full genomic sequences directly from bat specimens. We first present an overview of the available studies on bat CoVs, with details on their chiropteran hosts, then comparatively analyze the increase in bat CoV studies and novel genomic sequences obtained since the SARS pandemic. We then conduct a comprehensive phylogenetic analysis of the genera Alpha- and Betacoronavirus, to show that bats harbour more CoV diversity than other mammalian hosts and are widely represented in most, but not all parts of the tree of mammalian CoVs. We next discuss preliminary evidence for phylogenetic co-segregation of CoVs and bat hosts encompassing the Betacoronavirus clades b and d, with an emphasis on the sampling bias that exists among bat species and other mammals, then present examples of CoVs infecting different hosts on the one hand and viruses apparently confined to host genera on the other. We also demonstrate a geographic bias within available studies on bat CoVs, and identify a critical lack of information from biodiversity hotspots in Africa, Asia and Latin America. We then present evidence for a zoonotic origin of four of the six known human CoVs (HCoV), three of which likely involved bats, namely SARS-CoV, MERS-CoV and HCoV-229E; compare the available data on CoV pathogenesis in bats to that in other mammalian hosts; and discuss hypotheses on the putative insect origins of CoV ancestors. Finally, we suggest caution with conclusions on the zoonotic potential of bat viruses, based only on genomic sequence data, and emphasize the need to preserve these ecologically highly relevant animals. This paper forms part of a symposium in Antiviral Research on "from SARS to MERS: 10years of research on highly pathogenic human coronaviruses".

Keywords: Alphacoronavirus; Bats; Betacoronavirus; Coronaviridae; Taxonomy; Zoonosis.

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Figures

Fig. 1
Fig. 1
Coronavirus data in public databases. Panels A and B. Data was based on a GenBank search using the terms “Coronaviridae” [ORGANISM] AND Host [All Fields]” in the “Nucleotide” database, on June 16th, 2013. Panel C, PubMed data was retrieved from a search using the terms “coronaviruses, coronavirus, coronaviridae, coronavirinae, bat, chiroptera, bats”, on June 16th, 2013.
Fig. 2
Fig. 2
Phylogenetic relationships in the subfamily Coronavirinae. Bayesian phylogeny of an 816-nucleotide RNA-dependent RNA polymerase fragment, as described previously (Drexler et al., 2010) of the subfamily Coronavirinae using MrBayes V3.1 (Ronquist and Huelsenbeck, 2003) under assumption of a GTR + G + I substitution model, using 2,000,000 trees sampled every 100 steps, annotated with a burn-in of 25% using TreeAnnotator V1.7.4 and visualized using FigTree V1.4 from the BEAST package (Drummond et al., 2012). Cavally virus (Zirkel et al., 2011) was used as an outgroup. Values at deep nodes indicate statistical support from Bayesian posterior probabilities, scale bar genetic distance.
Fig. 3
Fig. 3
Phylogenetic relationships between coronaviruses and bat hosts. Details of the phylogeny shown in Fig. 2 for the genera Alpha- and Betacoronavirus. ICTV species are given to the right of clade designations and bat symbols, when applicable. Virus designations include strain names, GenBank accession numbers and host information as the first three letters of the latin genus and species names. Bat viruses are shown in red. Boxes indicate Alpha- and Betacoronavirus genera, according to the coloring in Fig. 2.
Fig. 4
Fig. 4
Bat families in which coronaviruses have been detected. Phylogeny of extant bat families is shown according to (Simmons, 2005). Boxes indicate descriptions of alpha- and betacoronaviruses according to the coloring in Fig. 2.
Fig. 5
Fig. 5
Distribution of bat coronavirus studies. Studies reporting bat CoV sequences by country are indicated, with the number of studies given in blue circles and adjusted in size accordingly. Country codes: BRA = Brazil, CAN = Canada, CRC = Costa Rica, MEX = Mexico, PAN = Panama, TRI = Trinidad and Tobago, USA = United States of America, BGR = Bulgaria, GBR = Great Britain, GER = Germany, ITA = Italy, NED = Netherlands, ROU = Romania, SLO = Slovenia, SPA = Spain, UKR = Ukraine, GHA = Ghana, KEN = Kenia, NGR = Nigeria, RCA = South African Republic, CHN = China, JPN = Japan, PHI = Philippines, THA = Thailand. The black circles for the Central African Republic (CAF), Gabon (GAB) and Australia (AUS) indicate published sequences in GenBank, but lack of publication of the corresponding studies. Countries where CoV studies have been performed are in black, others in grey.
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