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      From People to Panthera: Natural SARS-CoV-2 Infection in Tigers and Lions at the Bronx Zoo

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      mBio
      American Society for Microbiology
      One Health, Panthera leo, Panthera tigris, SARS-CoV-2, in situ hybridization, lion, rRT-PCR, tiger, virus isolation, whole-genome sequencing, zoo, zoonotic infection

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          Abstract

          The human-animal-environment interface of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an important aspect of the coronavirus disease 2019 (COVID-19) pandemic that requires robust One Health-based investigations. Despite this, few reports describe natural infections in animals or directly link them to human infections using genomic data. In the present study, we describe the first cases of natural SARS-CoV-2 infection in tigers and lions in the United States and provide epidemiological and genetic evidence for human-to-animal transmission of the virus. Our data show that tigers and lions were infected with different genotypes of SARS-CoV-2, indicating two independent transmission events to the animals. Importantly, infected animals shed infectious virus in respiratory secretions and feces. A better understanding of the susceptibility of animal species to SARS-CoV-2 may help to elucidate transmission mechanisms and identify potential reservoirs and sources of infection that are important in both animal and human health.

          ABSTRACT

          Despite numerous barriers to transmission, zoonoses are the major cause of emerging infectious diseases in humans. Among these, severe acute respiratory syndrome (SARS), Middle East respiratory syndrome (MERS), and ebolaviruses have killed thousands; the human immunodeficiency virus (HIV) has killed millions. Zoonoses and human-to-animal cross-species transmission are driven by human actions and have important management, conservation, and public health implications. The current SARS-CoV-2 pandemic, which presumably originated from an animal reservoir, has killed more than half a million people around the world and cases continue to rise. In March 2020, New York City was a global epicenter for SARS-CoV-2 infections. During this time, four tigers and three lions at the Bronx Zoo, NY, developed mild, abnormal respiratory signs. We detected SARS-CoV-2 RNA in respiratory secretions and/or feces from all seven animals, live virus in three, and colocalized viral RNA with cellular damage in one. We produced nine whole SARS-CoV-2 genomes from the animals and keepers and identified different SARS-CoV-2 genotypes in the tigers and lions. Epidemiologic and genomic data indicated human-to-tiger transmission. These were the first confirmed cases of natural SARS-CoV-2 animal infections in the United States and the first in nondomestic species in the world. We highlight disease transmission at a nontraditional interface and provide information that contributes to understanding SARS-CoV-2 transmission across species.

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          A Novel Coronavirus from Patients with Pneumonia in China, 2019

          Summary In December 2019, a cluster of patients with pneumonia of unknown cause was linked to a seafood wholesale market in Wuhan, China. A previously unknown betacoronavirus was discovered through the use of unbiased sequencing in samples from patients with pneumonia. Human airway epithelial cells were used to isolate a novel coronavirus, named 2019-nCoV, which formed a clade within the subgenus sarbecovirus, Orthocoronavirinae subfamily. Different from both MERS-CoV and SARS-CoV, 2019-nCoV is the seventh member of the family of coronaviruses that infect humans. Enhanced surveillance and further investigation are ongoing. (Funded by the National Key Research and Development Program of China and the National Major Project for Control and Prevention of Infectious Disease in China.)
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            MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

            We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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              A pneumonia outbreak associated with a new coronavirus of probable bat origin

              Since the outbreak of severe acute respiratory syndrome (SARS) 18 years ago, a large number of SARS-related coronaviruses (SARSr-CoVs) have been discovered in their natural reservoir host, bats 1–4 . Previous studies have shown that some bat SARSr-CoVs have the potential to infect humans 5–7 . Here we report the identification and characterization of a new coronavirus (2019-nCoV), which caused an epidemic of acute respiratory syndrome in humans in Wuhan, China. The epidemic, which started on 12 December 2019, had caused 2,794 laboratory-confirmed infections including 80 deaths by 26 January 2020. Full-length genome sequences were obtained from five patients at an early stage of the outbreak. The sequences are almost identical and share 79.6% sequence identity to SARS-CoV. Furthermore, we show that 2019-nCoV is 96% identical at the whole-genome level to a bat coronavirus. Pairwise protein sequence analysis of seven conserved non-structural proteins domains show that this virus belongs to the species of SARSr-CoV. In addition, 2019-nCoV virus isolated from the bronchoalveolar lavage fluid of a critically ill patient could be neutralized by sera from several patients. Notably, we confirmed that 2019-nCoV uses the same cell entry receptor—angiotensin converting enzyme II (ACE2)—as SARS-CoV.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mBio
                mBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                13 October 2020
                Sep-Oct 2020
                : 11
                : 5
                : e02220-20
                Affiliations
                [a ]Wildlife Conservation Society, Bronx Zoo, Bronx, New York, USA
                [b ]Department of Population Medicine and Diagnostic Sciences, Animal Health Diagnostic Center, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA
                [c ]Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA
                [d ]National Veterinary Services Laboratories, Animal and Plant Health Inspection Service (APHIS), U.S. Department of Agriculture (USDA), Ames, Iowa, USA
                [e ]Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois, USA
                [f ]Centers for Disease Control and Prevention, Atlanta, Georgia, USA
                [g ]Zoological Pathology Program, College of Veterinary Medicine, University of Illinois, Brookfield, Illinois, USA
                [h ]Chicago Zoological Society, Chicago, Illinois, USA
                [i ]New York State Department of Agriculture and Markets, Albany, New York, USA
                [j ]New York City Department of Health and Mental Hygiene, Queens, New York, USA
                Virginia Polytechnic Institute and State University
                Author notes
                Address correspondence to Denise McAloose, dmcaloose@ 123456wcs.org , or Diego G. Diel, dgdiel@ 123456cornell.edu .
                [*]

                Present address: Stephanie Zec, Dickerson Park Zoo, Springfield, Missouri, USA; Marina Ivančić, ZooRadOne, Chicago, Illinois, USA.

                Denise McAloose, Melissa Laverack, Leyi Wang, and Mary Lea Killian contributed equally to this work. Author order was agreed upon by all authors.

                Paul P. Calle, Karen Terio, Mia Kim Torchetti, and Diego G. Diel contributed equally to this work. Author order was agreed upon by all authors.

                Author information
                https://orcid.org/0000-0002-3945-3862
                https://orcid.org/0000-0002-3807-2339
                https://orcid.org/0000-0002-8327-3092
                https://orcid.org/0000-0003-3237-8940
                Article
                mBio02220-20
                10.1128/mBio.02220-20
                7554670
                33051368
                9fbb8a63-42aa-4e08-90c0-ae3d711427a8
                Copyright © 2020 McAloose et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 10 August 2020
                : 2 September 2020
                Page count
                supplementary-material: 10, Figures: 4, Tables: 0, Equations: 0, References: 42, Pages: 13, Words: 10090
                Funding
                Funded by: USDA | National Institute of Food and Agriculture (NIFA), https://doi.org/10.13039/100005825;
                Award ID: 2018-37620-28832
                Award Recipient :
                Funded by: U.S. Department of Agriculture (USDA), https://doi.org/10.13039/100000199;
                Award ID: AP19 VS NVSL00C020
                Award Recipient :
                Funded by: U.S. Department of Agriculture (USDA), https://doi.org/10.13039/100000199;
                Award ID: AP20 VS DB000C020
                Award Recipient :
                Funded by: HHS | U.S. Food and Drug Administration (FDA), https://doi.org/10.13039/100000038;
                Award ID: 1U18FD006866-01
                Award Recipient :
                Funded by: HHS | U.S. Food and Drug Administration (FDA), https://doi.org/10.13039/100000038;
                Award ID: 1U18FD006714-01
                Award Recipient :
                Funded by: HHS | U.S. Food and Drug Administration (FDA), https://doi.org/10.13039/100000038;
                Award ID: 1U18FD006716-01
                Award Recipient :
                Funded by: HHS | U.S. Food and Drug Administration (FDA), https://doi.org/10.13039/100000038;
                Award ID: 1U18FD006673-01
                Award Recipient :
                Categories
                Research Article
                Host-Microbe Biology
                Editor's Pick
                Custom metadata
                September/October 2020

                Life sciences
                one health,panthera leo,panthera tigris,sars-cov-2,in situ hybridization,lion,rrt-pcr,tiger,virus isolation,whole-genome sequencing,zoo,zoonotic infection

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