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Bat coronaviruses related to SARS-CoV-2 and infectious for human cells

Author

Listed:
  • Sarah Temmam

    (Université de Paris, Pathogen Discovery Laboratory
    Université de Paris, The OIE Collaborating Center for the Detection and Identification in Humans of Emerging Animal Pathogens)

  • Khamsing Vongphayloth

    (Institut Pasteur du Laos)

  • Eduard Baquero

    (Université de Paris, CNRS UMR 3569, Structural Virology Unit)

  • Sandie Munier

    (Université de Paris, CNRS UMR 3569, Molecular Genetics of RNA Viruses Unit)

  • Massimiliano Bonomi

    (Université de Paris, CNRS UMR 3528, Structural Bioinformatics Unit)

  • Béatrice Regnault

    (Université de Paris, Pathogen Discovery Laboratory
    Université de Paris, The OIE Collaborating Center for the Detection and Identification in Humans of Emerging Animal Pathogens)

  • Bounsavane Douangboubpha

    (National University of Laos)

  • Yasaman Karami

    (Université de Paris, CNRS UMR 3528, Structural Bioinformatics Unit)

  • Delphine Chrétien

    (Université de Paris, Pathogen Discovery Laboratory
    Université de Paris, The OIE Collaborating Center for the Detection and Identification in Humans of Emerging Animal Pathogens)

  • Daosavanh Sanamxay

    (National University of Laos)

  • Vilakhan Xayaphet

    (National University of Laos)

  • Phetphoumin Paphaphanh

    (National University of Laos)

  • Vincent Lacoste

    (Institut Pasteur du Laos)

  • Somphavanh Somlor

    (Institut Pasteur du Laos)

  • Khaithong Lakeomany

    (Institut Pasteur du Laos)

  • Nothasin Phommavanh

    (Institut Pasteur du Laos)

  • Philippe Pérot

    (Université de Paris, Pathogen Discovery Laboratory
    Université de Paris, The OIE Collaborating Center for the Detection and Identification in Humans of Emerging Animal Pathogens)

  • Océane Dehan

    (Université de Paris, CNRS UMR 3569, Molecular Genetics of RNA Viruses Unit
    Université de Paris, National Reference Center for Respiratory Viruses)

  • Faustine Amara

    (Université de Paris, CNRS UMR 3569, Molecular Genetics of RNA Viruses Unit)

  • Flora Donati

    (Université de Paris, CNRS UMR 3569, Molecular Genetics of RNA Viruses Unit
    Université de Paris, National Reference Center for Respiratory Viruses)

  • Thomas Bigot

    (Université de Paris, Pathogen Discovery Laboratory
    Université de Paris, Bioinformatic and Biostatistic Hub - Computational Biology Department)

  • Michael Nilges

    (Université de Paris, CNRS UMR 3528, Structural Bioinformatics Unit)

  • Félix A. Rey

    (Université de Paris, CNRS UMR 3569, Structural Virology Unit)

  • Sylvie van der Werf

    (Université de Paris, CNRS UMR 3569, Molecular Genetics of RNA Viruses Unit
    Université de Paris, National Reference Center for Respiratory Viruses)

  • Paul T. Brey

    (Institut Pasteur du Laos)

  • Marc Eloit

    (Université de Paris, Pathogen Discovery Laboratory
    Université de Paris, The OIE Collaborating Center for the Detection and Identification in Humans of Emerging Animal Pathogens
    Ecole Nationale Vétérinaire d’Alfort, University of Paris-Est)

Abstract

The animal reservoir of SARS-CoV-2 is unknown despite reports of SARS-CoV-2-related viruses in Asian Rhinolophus bats1–4, including the closest virus from R. affinis, RaTG13 (refs. 5,6), and pangolins7–9. SARS-CoV-2 has a mosaic genome, to which different progenitors contribute. The spike sequence determines the binding affinity and accessibility of its receptor-binding domain to the cellular angiotensin-converting enzyme 2 (ACE2) receptor and is responsible for host range10–12. SARS-CoV-2 progenitor bat viruses genetically close to SARS-CoV-2 and able to enter human cells through a human ACE2 (hACE2) pathway have not yet been identified, although they would be key in understanding the origin of the epidemic. Here we show that such viruses circulate in cave bats living in the limestone karstic terrain in northern Laos, in the Indochinese peninsula. We found that the receptor-binding domains of these viruses differ from that of SARS-CoV-2 by only one or two residues at the interface with ACE2, bind more efficiently to the hACE2 protein than that of the SARS-CoV-2 strain isolated in Wuhan from early human cases, and mediate hACE2-dependent entry and replication in human cells, which is inhibited by antibodies that neutralize SARS-CoV-2. None of these bat viruses contains a furin cleavage site in the spike protein. Our findings therefore indicate that bat-borne SARS-CoV-2-like viruses that are potentially infectious for humans circulate in Rhinolophus spp. in the Indochinese peninsula.

Suggested Citation

  • Sarah Temmam & Khamsing Vongphayloth & Eduard Baquero & Sandie Munier & Massimiliano Bonomi & Béatrice Regnault & Bounsavane Douangboubpha & Yasaman Karami & Delphine Chrétien & Daosavanh Sanamxay & V, 2022. "Bat coronaviruses related to SARS-CoV-2 and infectious for human cells," Nature, Nature, vol. 604(7905), pages 330-336, April.
    • Handle: RePEc:nat:nature:v:604:y:2022:i:7905:d:10.1038_s41586-022-04532-4
    DOI: 10.1038/s41586-022-04532-4
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    Cited by:

    1. Jun-Yu Si & Yuan-Mei Chen & Ye-Hui Sun & Meng-Xue Gu & Mei-Ling Huang & Lu-Lu Shi & Xiao Yu & Xiao Yang & Qing Xiong & Cheng-Bao Ma & Peng Liu & Zheng-Li Shi & Huan Yan, 2024. "Sarbecovirus RBD indels and specific residues dictating multi-species ACE2 adaptiveness," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Anna S. Speranskaya & Ilia V. Artiushin & Andrei E. Samoilov & Elena V. Korneenko & Kirill V. Khabudaev & Elena N. Ilina & Alexander P. Yusefovich & Marina V. Safonova & Anna S. Dolgova & Anna S. Glad, 2023. "Identification and Genetic Characterization of MERS-Related Coronavirus Isolated from Nathusius’ Pipistrelle ( Pipistrellus nathusii ) near Zvenigorod (Moscow Region, Russia)," IJERPH, MDPI, vol. 20(4), pages 1-16, February.
    3. Wenjuan Du & Oliver Debski-Antoniak & Dubravka Drabek & Rien Haperen & Melissa Dortmondt & Joline Lee & Ieva Drulyte & Frank J. M. Kuppeveld & Frank Grosveld & Daniel L. Hurdiss & Berend-Jan Bosch, 2024. "Neutralizing antibodies reveal cryptic vulnerabilities and interdomain crosstalk in the porcine deltacoronavirus spike protein," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Jing Wang & Yuan-fei Pan & Li-fen Yang & Wei-hong Yang & Kexin Lv & Chu-ming Luo & Juan Wang & Guo-peng Kuang & Wei-chen Wu & Qin-yu Gou & Gen-yang Xin & Bo Li & Huan-le Luo & Shoudeng Chen & Yue-long, 2023. "Individual bat virome analysis reveals co-infection and spillover among bats and virus zoonotic potential," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Juan Liu & Fengfeng Mao & Jianhe Chen & Shuaiyao Lu & Yonghe Qi & Yinyan Sun & Linqiang Fang & Man Lung Yeung & Chunmei Liu & Guimei Yu & Guangyu Li & Ximing Liu & Yuansheng Yao & Panpan Huang & Dongx, 2023. "An IgM-like inhalable ACE2 fusion protein broadly neutralizes SARS-CoV-2 variants," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Yelin Han & Panpan Xu & Yuyang Wang & Wenliang Zhao & Junpeng Zhang & Shuyi Zhang & Jianwei Wang & Qi Jin & Zhiqiang Wu, 2023. "Panoramic analysis of coronaviruses carried by representative bat species in Southern China to better understand the coronavirus sphere," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    7. David Hueting & Karen Schriever & Rui Sun & Stelios Vlachiotis & Fanglei Zuo & Likun Du & Helena Persson & Camilla Hofström & Mats Ohlin & Karin Walldén & Marcus Buggert & Lennart Hammarström & Harold, 2023. "Design, structure and plasma binding of ancestral β-CoV scaffold antigens," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    8. Susanne Kessler & Bradly Burke & Geoffroy Andrieux & Jan Schinköthe & Lea Hamberger & Johannes Kacza & Shijun Zhan & Clara Reasoner & Taru S. Dutt & Maria Kaukab Osman & Marcela Henao-Tamayo & Julian , 2024. "Deciphering bat influenza H18N11 infection dynamics in male Jamaican fruit bats on a single-cell level," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    9. Cedric C. S. Tan & Jahcub Trew & Thomas P. Peacock & Kai Yi Mok & Charlie Hart & Kelvin Lau & Dongchun Ni & C. David L. Orme & Emma Ransome & William D. Pearse & Christopher M. Coleman & Dalan Bailey , 2023. "Genomic screening of 16 UK native bat species through conservationist networks uncovers coronaviruses with zoonotic potential," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Luo-Yuan Xia & Zhen-Fei Wang & Xiao-Ming Cui & Yuan-Guo Li & Run-Ze Ye & Dai-Yun Zhu & Fang-Xu Li & Jie Zhang & Wen-Hao Wang & Ming-Zhu Zhang & Wan-Ying Gao & Lian-Feng Li & Teng-Cheng Que & Tie-Cheng, 2024. "Isolation and characterization of a pangolin-borne HKU4-related coronavirus that potentially infects human-DPP4-transgenic mice," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    11. Renata L. Muylaert & David A. Wilkinson & Tigga Kingston & Paolo D’Odorico & Maria Cristina Rulli & Nikolas Galli & Reju Sam John & Phillip Alviola & David T. S. Hayman, 2023. "Using drivers and transmission pathways to identify SARS-like coronavirus spillover risk hotspots," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Peter J. Halfmann & Kathryn Loeffler & Augustine Duffy & Makoto Kuroda & Jie E. Yang & Elizabeth R. Wright & Yoshihiro Kawaoka & Ravi S. Kane, 2024. "Broad protection against clade 1 sarbecoviruses after a single immunization with cocktail spike-protein-nanoparticle vaccine," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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