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Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor
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The 2002-3 pandemic caused by severe acute respiratory syndrome coronavirus (SARS-CoV) was one of the most significant public health events in recent history. An ongoing outbreak of Middle East respiratory syndrome coronavirus suggests that this group of viruses remains a key threat and that their distribution is wider than previously recognized. Although bats have been suggested to be the natural reservoirs of both viruses, attempts to isolate the progenitor virus of SARS-CoV from bats have been unsuccessful. Diverse SARS-like coronaviruses (SL-CoVs) have now been reported from bats in China, Europe and Africa, but none is considered a direct progenitor of SARS-CoV because of their phylogenetic disparity from this virus and the inability of their spike proteins to use the SARS-CoV cellular receptor molecule, the human angiotensin converting enzyme II (ACE2). Here we report whole-genome sequences of two novel bat coronaviruses from Chinese horseshoe bats (family: Rhinolophidae) in Yunnan, China: RsSHC014 and Rs3367. These viruses are far more closely related to SARS-CoV than any previously identified bat coronaviruses, particularly in the receptor binding domain of the spike protein. Most importantly, we report the first recorded isolation of a live SL-CoV (bat SL-CoV-WIV1) from bat faecal samples in Vero E6 cells, which has typical coronavirus morphology, 99.9% sequence identity to Rs3367 and uses ACE2 from humans, civets and Chinese horseshoe bats for cell entry. Preliminary in vitro testing indicates that WIV1 also has a broad species tropism. Our results provide the strongest evidence to date that Chinese horseshoe bats are natural reservoirs of SARS-CoV, and that intermediate hosts may not be necessary for direct human infection by some bat SL-CoVs. They also highlight the importance of pathogen-discovery programs targeting high-risk wildlife groups in emerging disease hotspots as a strategy for pandemic preparedness.
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“SARS-related coronaviruses appear frequently in bats (proximal source) [30].”
From Waves and variants of SARS-CoV-2: understanding the causes and effect of the COVID-19 catastrophe (2022) · cites this paper as [30]
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Shehata, A. A., Attia, Y. A., Rahman, M. T., Basiouni, S., El-Seedi, H. R., Azhar, E. I., Khafaga, A. F., & Hafez, H. M. (2022) · Animals · doi:10.3390/ani12030378 · Cited by 30
Severe zoonotic viruses carried by different species of bats and their regional distribution
Liu, Z., Liu, Q., Wang, H., & Yao, X. (2023) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2023.09.025 · Cited by 29
Fugong virus, a novel hantavirus harbored by the small oriental vole (Eothenomys eleusis) in China
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Transmission Cycle of SARS-CoV and SARS-CoV-2
Yadav, T., & Saxena, S. K. (2020) · Medical virology · doi:10.1007/978-981-15-4814-7_4 · Cited by 34
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“SARS-CoV-2, the causative agent for COVID-19 [57], enters its host cell by binding to angiotensin-converting enzyme 2 (ACE2) receptors, which are prevalent on the mucosal surface (Table 1) [58].”
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Desterke, C., Griscelli, F., Imeri, J., Marcoux, P. J., Lemonnier, T., Latsis, T., Turhan, A. G., & Griscelli, A. B. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.20-0189 · Cited by 29
“The bat SARS-like coronavirus COVID-19 uses the angiotensin converting enzyme receptor 2 (ACE2) to enter the cells.(2) ACE2 is highly distributed in all adult cells, including lung, heart, kidney, liver, and endothelial cells that are then highly susceptible to infection by COVID-19, which uses its S protein for this…”
Adu-Agyeiwaah, Y., Grant, M. B., & Obukhov, A. G. (2020) · Cells · doi:10.3390/cells9112528 · Cited by 29
SARS-CoV-2, Early Entry Events
CHAMBERS, J. K., Yu, J., Valdés, J. J., & Arulanandam, B. P. (2020) · Journal of Pathogens · doi:10.1155/2020/9238696 · Cited by 32
Theoretical and numerical analysis of novel COVID-19 via fractional order mathematical model
Ali, A., Khan, M. Y., Sinan, M., Allehiany, F. M., Mahmoud, E. E., Abdel‐Aty, A., & Ali, G. (2020) · Results in Physics · doi:10.1016/j.rinp.2020.103676 · Cited by 29
“Researchers of related fields thinks that root cause of nCovid-2019, was first resulted due the bats, which are identical to that of SARS (Severe Acute Respiratory Syndromes), which took birth in China and the rest of the world in 2003 [6,7].”
The emerging SARS-CoV, MERS-CoV, and SARS-CoV-2: An insight into the viruses zoonotic aspects
Al-Salihi, K. A., & Khalaf, J. M. (2021) · Veterinary World · doi:10.14202/vetworld.2021.190-199 · Cited by 29
“They were also identified to harbor a large number of SARSrelated CoVs (SARSr-CoVs) [28,61,75].”
BackgroundIllian, D. N., Siregar, E. S., Sumaiyah, S., Utomo, A. R. H., Nuryawan, A., & Basyuni, M. (2021) · Heliyon · doi:10.1016/j.heliyon.2021.e06001 · Cited by 29
“SARS-CoV-2 interacts with cell surface receptors named angiotensin converting enzyme 2 (ACE-2) once it enters the cells of humans (Li et al., 2003; Han et al., 2006; Ge et al., 2013).”
BackgroundIs lymphopenia different between SARS and COVID‐19 patients?
Yan, S., & Wu, G. (2021) · The FASEB Journal · doi:10.1096/fj.202002512 · Cited by 28
Medicinal and therapeutic potential of withanolides from Withania somnifera against COVID-19
Dhawan, M. K., Manisha, P., Sharun, K., Tiwari, R., Bilal, M., & Dhama, K. (2021) · Journal of Applied Pharmaceutical Science · doi:10.7324/japs.2021.110402 · Cited by 32
Human cell receptors: potential drug targets to combat COVID-19
Raghav, P. K., Kalyanaraman, K., & Kumar, D. (2021) · Amino Acids · doi:10.1007/s00726-021-02991-z · Cited by 29
“The function of these mutations in viral pathogenicity must be further investigated (Petrosillo et al. 2020; Wu et al. 2020; Ge et al. 2013).”
BackgroundCOVID-19: Invasion, pathogenesis and possible cure – A review
Nitin, P., Nandhakumar, R., Vidhya, B., Rajesh, S., & Ayyasamy, S. (2021) · Journal of Virological Methods · doi:10.1016/j.jviromet.2021.114434 · Cited by 30
Dahiya, S., Luetkens, T., Lutfi, F. U., Avila, S. V., Iraguha, T., Margiotta, P., Hankey, K. G., Lesho, P., Law, J. Y., Lee, S. T., et al. (2021) · Blood Advances · doi:10.1182/bloodadvances.2021006112 · Cited by 29
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Self-citationGhufran, M., Ullah, M., Khan, H. A., Ghufran, S., Ayaz, M., Siddiq, M., Abbas, S. Q., Hassan, S. S. U., & BUNGAU, S. G. (2023) · Bioengineering · doi:10.3390/bioengineering10010100 · Cited by 29
“The S spike protein binds to the angiotensin-converting enzyme 2 (ACE2) receptor on mammalian lung cells, allowing the virus’s RNA genetic material to be released into the host cells [10].”
BackgroundThe diversity of the glycan shield of sarbecoviruses related to SARS-CoV-2
Allen, J. D., Ivory, D. P., Song, G., He, W., Capozzola, T., Yong, P., Burton, D. R., Andrabi, R., & Crispin, M. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112307 · Cited by 32
Detection of coronavirus genomes in Moluccan naked-backed fruit bats in Indonesia
Anindita, P. D., Sasaki, M., Setiyono, A., Handharyani, E., Orba, Y., Kobayashi, S., Rahmadani, I., Taha, S. R., Adiani, S., Subangkit, M., et al. (2015) · Archives of Virology · doi:10.1007/s00705-015-2342-1 · Cited by 29
Ji, H., de Souza, A. M. A., Bajaj, B., Zheng, W., Wu, X., Speth, R. C., & Sandberg, K. L. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.15276 · Cited by 29
“In 2003, ACE2 was discovered to be the severe acute respiratory syndrome coronavirus (SARS-CoV) receptor.(6,7) Molecular modeling studies indicate the structure of SARS-CoV-2—the virus underlying the current coronavirus disease 2019 (COVID19) pandemic—has even higher affinity for ACE2 than SARSCoV.”
BackgroundSarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness
Si, J.-Y., Chen, Y.-M., Sun, Y.-H., Gu, M.-X., Huang, M.-L., Shi, L.-L., Yu, X., Yang, X., Xiong, Q., Ma, C.-B., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-53029-3 · Cited by 25
“Nevertheless, ACE2 usage has been demonstrated in most representative sarbecoviruses other than clade 2 sarbecoviruses 3,6,7,16,22,26 .”
Self-citationDisease tolerance as immune defense strategy in bats: One size fits all?
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Overview of COVID-19 and neurological complications
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Evolution, Ecology, and Zoonotic Transmission of Betacoronaviruses: A Review
Jelinek, H. F., Mousa, M., Alefishat, E. A., Osman, W. M., Spence, I., Bu, D., Feng, S. F., Byrd, J. H., Magni, P. A., Sahibzada, S., et al. (2021) · Frontiers in Veterinary Science · doi:10.3389/fvets.2021.644414 · Cited by 28
“Sci. 8:644414. doi: 10.3389/fvets.2021.644414 Evolution, Ecology, and Zoonotic Transmission of Betacoronaviruses: A Review Herbert F. Jelinek 1,2,3, Mira Mousa 4, Eman Alefishat 1,5,6, Wael Osman 7, Ian Spence 8, Dengpan Bu 9, Samuel F. Feng 1,10, Jason Byrd 11, Paola A. Magni 12,13, Shafi Sahibzada 14, Guan K. Tay 1,…”
BackgroundInfluentialComputational studies on phylogeny and drug designing using molecular simulations for COVID-19
Nabi, F., Ahmad, O., Khan, Y. A., Nabi, A., Hashmi, M. A., Qais, F. A., Masroor, A., Hisamuddin, M., Uversky, V. N., & Khan, R. H. (2021) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2021.1947895 · Cited by 28
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“Despite the discovery of many bat coronaviruses, only a couple of them have been successfully isolated and cultivated or propagated from molecularly engineered viruses.(5,33) A lineage C beta-coronavirus Tylonycteris pachypus coronavirus HKU4 (CoV-HKU4) is one of the cultivable bat coronaviruses, probably owing to its…”
BackgroundA Glimpse on the Evolution of RNA Viruses: Implications and Lessons from SARS-CoV-2
Šimičić, P., & Lepej, S. Ž. (2022) · Viruses · doi:10.3390/v15010001 · Cited by 30
Metadata
- Authors
- Ge, X.-Y., Li, J.-L., Yang, X.-L., Chmura, A. A., Zhu, G., Epstein, J. H., Mazet, J. K., Hu, B., Zhang, W., Peng, C., Zhang, Y.-J., Luo, C.-M., Tan, B., Wang, N., Zhu, Y., Crameri, G., Zhang, S.-Y., Wang, L.-F., Daszak, P., & Shi, Z.-L.
- Affiliations
- Chinese Academy of Sciences (CN)
- EcoHealth Alliance (US)
- Commonwealth Scientific and Industrial Research Organisation (AU)
- Corresponding author
- Daszak, Peter
- Shi, Zheng-Li
- ORCID
- Venue
- Nature
- Published
- 2013-10-30
- Volume
- 503
- Issue
- 7477
- Pages
- 535-538
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5389864
- OpenAlex
- W1993577573
- Cited by
- 1,778
- References
- 30
- Citations by year
- 2026: 39 · 2025: 67 · 2024: 83 · 2023: 120 · 2022: 205 · 2021: 356 · 2020: 580 · 2019: 48 · 2018: 46 · 2017: 54 · 2016: 60 · 2015: 55 · 2014: 55 · 2013: 7
- FWCI
- 43.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Commons - University of South Florida (University of South Florida) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- U.S. Department of Health and Human Services
- United States Agency for International Development
- Commonwealth Scientific and Industrial Research Organisation
- National Natural Science Foundation of China (2013FY113500, 81290341, 2010CB530100, 31321001)
- Southern Medical University
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (R01AI110964, R01AI079231)
- Fogarty International Center (R01TW005869, R56TW009502)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Zoonotic diseases and public health
- Keywords
- SARS-like coronaviruses, bat coronaviruses, Chinese horseshoe bat, horseshoe bats, ACE2 receptor, bat-to-human transmission, spike protein receptor-binding domain, MERS-CoV, coronavirus phylogeny, Yunnan
- MeSH terms
- Angiotensin-Converting Enzyme 2, Animals, Chlorocebus aethiops, China, Chiroptera, Disease Reservoirs, Feces, Fluorescent Antibody Technique, Humans, Peptidyl-Dipeptidase A, Molecular Sequence Data, Receptors, Virus, Species Specificity, Vero Cells, Virion, Genome, Viral, Severe Acute Respiratory Syndrome, Severe acute respiratory syndrome-related coronavirus, Viverridae, Virus Internalization, Host Specificity, Pandemics, Real-Time Polymerase Chain Reaction, Spike Glycoprotein, Coronavirus
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