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The Discovery of Bombali Virus Adds Further Support for Bats As Hosts of Ebolaviruses

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The Discovery of Bombali Virus Adds Further Support for Bats As Hosts of Ebolaviruses BRIEF COMMUNICATION https://doi.org/10.1038/s41564-018-0227-2 The discovery of Bombali virus adds further support for bats as hosts of ebolaviruses Tracey Goldstein 1,14*, Simon J. Anthony2,3,4,14*, Aiah Gbakima5, Brian H. Bird1, James Bangura5, Alexandre Tremeau-Bravard1, Manjunatha N. Belaganahalli 1, Heather L. Wells 2, Jasjeet K. Dhanota 1, Eliza Liang2,4, Michael Grodus2, Rohit K. Jangra6, Veronica A. DeJesus6, Gorka Lasso7, Brett R. Smith1, Amara Jambai8, Brima O. Kamara9, Sorie Kamara10, William Bangura11, Corina Monagin1,12, Sagi Shapira7,13, Christine K. Johnson1, Karen Saylors12, Edward M. Rubin12, Kartik Chandran6, W. Ian Lipkin2,3 and Jonna A. K. Mazet1 Here we describe the complete genome of a new ebolavirus, also positive using a separate ebolavirus ‘genus-level’ cPCR assay. Bombali virus (BOMV) detected in free-tailed bats in Sierra The resulting 187-bp fragment showed 83% nucleotide identity Leone (little free-tailed (Chaerephon pumilus) and Angolan to known ebolaviruses. All samples collected from dogs, cats and free-tailed (Mops condylurus)). The bats were found roost- rodents were negative when both assays were used. Given the 2013 ing inside houses, indicating the potential for human trans- Ebola virus disease outbreak, we also screened all samples for EBOV mission. We show that the viral glycoprotein can mediate using specific real-time PCR (rtPCR); however, all samples, includ- entry into human cells. However, further studies are required ing those from bats, were negative. to investigate whether exposure has actually occurred or if All bats (n =​ 244) were barcoded to confirm the species BOMV is pathogenic in humans. (Supplementary Table 1). Of the four positive bats, three were iden- Ebolaviruses (family: Filoviridae) are non-segmented, negative- tified as little free-tailed bats (Chaerephon pumilus) based on 98% sense, single-stranded RNA viruses. Five species have been sequence identity in the MT-Cytb gene and 99% in the MT-CO1 described to date, for which the prototypic viruses are Zaire virus gene. The fourth bat was identified as an Angolan free-tailed bat (EBOV), Bundibugyo virus (BDBV), Sudan virus (SUDV), Taï (Mops condylurus) based on 98% identity in the MT-Cytb gene and Forest virus (TAFV) and Reston virus (RESTV)1. With the exception 99% in the MT-CO1 gene. These bats co-roost and are widely dis- of RESTV, all have been associated with severe disease in humans. tributed across Western and sub-Saharan Africa (Supplementary EBOV was the first ebolavirus described and since 1976 more than Figure 1). The four positive bats were adult females sampled between 25 outbreaks have been recognized2. The most significant outbreak the 21 and 28 May 2016 at three different sites within 20 km of occurred in Guinea, Sierra Leone and Liberia in 2013–2016 where each other in the Bombali District (Supplementary Figure 1). They an estimated 28,000 humans were infected and 11,325 died3. were sampled inside human dwellings in small villages, where ani- Despite more than 40 years of research and continued outbreaks, mals (poultry, goats, sheep) and crops (fruit, vegetables, oil trees) the reservoirs of EBOV and the other ebolaviruses remain unknown. were raised for local consumption and sale (Supplementary Table 2). Current evidence points to bats4–9, although failure to isolate a virus Using unbiased high-throughput sequencing, 98% of the genome or recover a complete genome means that no ebolavirus has been was recovered from the oral swab of the Angolan free-tailed bat conclusively linked to any particular bat species. Therefore, we ini- with an average depth of 12×. Using virome capture sequencing tiated a survey in Sierra Leone to identify hosts of EBOV as well as (VirCapSeq), 42% of the genome was recovered with an average any additional filoviruses that might be circulating in wildlife. depth of 5×. Gene walking using PCR and Sanger sequencing was Between March and September 2016, 1,278 samples were col- used to obtain a second genome from the rectal swab of a little free- lected from 535 animals (244 bats, 46 rodents, 240 dogs, 5 cats) tailed bat. The termini for both sequences were then verified using from 20 locations in Sierra Leone (Supplementary Figure 1). rapid amplification of cDNA ends (RACE) to generate two com- Three oral and two rectal swabs from four insectivorous bats were plete BOMV genomes (GenBank accession numbers: MF319185 positive using a broadly reactive filovirus ‘family-level’ consensus and MF319186). The two genomes share 99.1% sequence identity PCR (cPCR) assay (4/244, Supplementary Table 1). The resulting to each other. 680-bp fragment showed 75% nucleotide identity to other known Phylogenetic analyses showed that BOMV is sufficiently dis- ebolaviruses. Rectal swabs for two of the four positive bats were tinct to represent the prototypic strain of a new species within the 1One Health Institute & Karen C. Drayer Wildlife Health Center, School of Veterinary Medicine, University of California, Davis, CA, USA. 2Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, NY, USA. 3Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA. 4EcoHealth Alliance, New York, NY, USA. 5Metabiota, Inc. Sierra Leone, Freetown, Sierra Leone. 6Department of Microbiology and Immunology, Albert Einstein College of Medicine, New York, NY, USA. 7Department of Systems Biology, Irving Cancer Research Center, Columbia University, New York, NY, USA. 8Ministry of Health and Sanitation, Freetown, Sierra Leone. 9Ministry of Health and Sanitation, Makeni, Sierra Leone. 10Livestock and Veterinary Services Division, Ministry of Agriculture, Forestry and Food Security, Freetown, Sierra Leone. 11Forestry and Wildlife Division, Ministry of Agriculture, Forestry and Food Security, Freetown, Sierra Leone. 12Metabiota, Inc., San Francisco, CA, USA. 13Department of Microbiology & Immunology, Columbia University, New York, NY, USA. 14These authors contributed equally: Tracey Goldstein, Simon J. Anthony. *e-mail: [email protected]; [email protected] NatURE MicrobiologY | www.nature.com/naturemicrobiology BRIEF COMMUNICATION NATURE MICROBIOLOGY a b NP EBOV/H.sap/COD/76 VP35 EBOV/H.sap/COD/76 ω = 0.1708 EBOV/H.sap/COD/95 ω = 0.1540 EBOV/H.sap/COD/95 EBOV/H.sap/COD/07 EBOV/H.sap/LBR/14 EBOV/H.sap/GIN/14 EBOV/H.sap/GIN/14 EBOV/H.sap/LBR/14 EBOV/H.sap/SLE/15 1 1 EBOV/H.sap/SLE/15 EBOV/H.sap/COD/07 BDBV/H.sap/UGA/07 BDBV/H.sap/UGA/07 1 1 1 1 TAFV/H.sap/CIV/94 TAFV/H.sap/CIV/94 BOMV/M.con/SLE/16 BOMV/M.con/SLE/16 1 1 BOMV/C.pum/SLE/16 BOMV/C.pum/SLE/16 SUDV/H.sap/UGA/00 SUDV/H.sap/UGA/00 1 0.98 1 0.94 RESTV/M.fas/USA/89 RESTV/M.fas/USA/89 1 LLOV/M.sch/ESP/03 1 LLOV/M.sch/ESP/03 MARV/H.sap/COD/99 MARV/H.sap/COD/99 1 1 MARV/R.aeg/UGA/09 MARV/R.aeg/UGA/09 0.5 0.4 c VP40 EBOV/H.sap/COD/76 d GP EBOV/H.sap/COD/76 EBOV/H.sap/COD/95 EBOV/H.sap/COD/95 ω = 0.1096 ω = 0.2409 EBOV/H.sap/GIN/14 EBOV/H.sap/COD/07 EBOV/H.sap/LBR/14 EBOV/H.sap/LBR/14 EBOV/H.sap/SLE/15 EBOV/H.sap/GIN/14 1 EBOV/H.sap/COD/07 0.95 EBOV/H.sap/SLE/15 BDBV/H.sap/UGA/07 BDBV/H.sap/UGA/07 1 1 TAFV/H.sap/CIV/94 1 TAFV/H.sap/CIV/94 BOMV/M.con/SLE/16 BOMV/M.con/SLE/16 1 1 BOMV/C.pum/SLE/16 BOMV/C.pum/SLE/16 SUDV/H.sap/UGA/00 SUDV/H.sap/UGA/00 1 1 1 1 RESTV/M.fas/USA/89 RESTV/M.fas/USA/89 1 LLOV/M.sch/ESP/03 1 LLOV/M.sch/ESP/03 MARV/H.sap/COD/99 1MARV/H.sap/COD/99 1 MARV/R.aeg/UGA/09 MARV/R.aeg/UGA/09 0.5 0.4 e VP30 EBOV/H.sap/COD/76 f VP24 EBOV/H.sap/COD/76 EBOV/H.sap/COD/95 EBOV/H.sap/COD/95 ω = 0.1503 ω = 0.0874 EBOV/H.sap/GIN/14 EBOV/H.sap/LBR/14 EBOV/H.sap/SLE/15 EBOV/H.sap/GIN/14 EBOV/H.sap/LBR/14 EBOV/H.sap/SLE/15 1 EBOV/H.sap/COD/07 1 EBOV/H.sap/COD/07 BDBV/H.sap/UGA/07 BDBV/H.sap/UGA/07 0.99 1 1 TAFV/H.sap/CIV/94 0.98 TAFV/H.sap/CIV/94 0.73 SUDV/H.sap/UGA/00 0.64 BOMV/M.con/SLE/16 1 RESTV/M.fas/USA/89 BOMV/C.pum/SLE/16 BOMV/M.con/SLE/16 1 RESTV/M.fas/USA/89 1 BOMV/C.pum/SLE/16 1 SUDV/H.sap/UGA/00 1 LLOV/M.sch/ESP/03 1 LLOV/M.sch/ESP/03 MARV/H.sap/COD/99 MARV/H.sap/COD/99 1 1 MARV/R.aeg/UGA/09 MARV/R.aeg/UGA/09 0.3 0.2 g L EBOV/H.sap/COD/76 h Full genome EBOV/H.sap/COD/76 EBOV/H.sap/COD/95 EBOV/H.sap/COD/95 = 0.1206 ω EBOV/H.sap/COD/07 EBOV/H.sap/COD/07 EBOV/H.sap/LBR/14 EBOV/H.sap/LBR/14 EBOV/H.sap/GIN/14 EBOV/H.sap/GIN/14 1 1 EBOV/H.sap/SLE/15 EBOV/H.sap/SLE/15 BDBV/H.sap/UGA/07 BDBV/H.sap/UGA/07 1 1 1 1 TAFV/H.sap/CIV/94 TAFV/H.sap/CIV/94 BOMV/M.con/SLE/16 1 1 BOMV/M.con/SLE/16 BOMV/C.pum/SLE/16 BOMV/C.pum/SLE/16 SUDV/H.sap/UGA/00 SUDV/H.sap/UGA/00 1 1 1 1 RESTV/M.fas/USA/89 RESTV/M.fas/USA/89 1 LLOV/M.sch/ESP/03 1 LLOV/M.sch/ESP/03 MARV/H.sap/COD/99 MARV/H.sap/COD/99 1 1 MARV/R.aeg/UGA/09 MARV/R.aeg/UGA/09 0.3 0.4 Fig.
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