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Molecular Architecture of Early Dissemination and Massive Second Wave of the SARS-CoV-2 Virus in a Major Metropolitan Area.
mBio. 2020 10 30; 11(6)MBIO

Abstract

We sequenced the genomes of 5,085 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains causing two coronavirus disease 2019 (COVID-19) disease waves in metropolitan Houston, TX, an ethnically diverse region with 7 million residents. The genomes were from viruses recovered in the earliest recognized phase of the pandemic in Houston and from viruses recovered in an ongoing massive second wave of infections. The virus was originally introduced into Houston many times independently. Virtually all strains in the second wave have a Gly614 amino acid replacement in the spike protein, a polymorphism that has been linked to increased transmission and infectivity. Patients infected with the Gly614 variant strains had significantly higher virus loads in the nasopharynx on initial diagnosis. We found little evidence of a significant relationship between virus genotype and altered virulence, stressing the linkage between disease severity, underlying medical conditions, and host genetics. Some regions of the spike protein-the primary target of global vaccine efforts-are replete with amino acid replacements, perhaps indicating the action of selection. We exploited the genomic data to generate defined single amino acid replacements in the receptor binding domain of spike protein that, importantly, produced decreased recognition by the neutralizing monoclonal antibody CR3022. Our report represents the first analysis of the molecular architecture of SARS-CoV-2 in two infection waves in a major metropolitan region. The findings will help us to understand the origin, composition, and trajectory of future infection waves and the potential effect of the host immune response and therapeutic maneuvers on SARS-CoV-2 evolution.IMPORTANCE There is concern about second and subsequent waves of COVID-19 caused by the SARS-CoV-2 coronavirus occurring in communities globally that had an initial disease wave. Metropolitan Houston, TX, with a population of 7 million, is experiencing a massive second disease wave that began in late May 2020. To understand SARS-CoV-2 molecular population genomic architecture and evolution and the relationship between virus genotypes and patient features, we sequenced the genomes of 5,085 SARS-CoV-2 strains from these two waves. Our report provides the first molecular characterization of SARS-CoV-2 strains causing two distinct COVID-19 disease waves.

Authors+Show Affiliations

Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA. Department of Pathology and Laboratory Medicine, Weill Cornell Medical College, New York, New York, USA. Department of Microbiology and Immunology, Weill Cornell Medical College, New York, New York, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA. Department of Pathology and Laboratory Medicine, Weill Cornell Medical College, New York, New York, USA. Department of Microbiology and Immunology, Weill Cornell Medical College, New York, New York, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA. Department of Pathology and Laboratory Medicine, Weill Cornell Medical College, New York, New York, USA. Department of Microbiology and Immunology, Weill Cornell Medical College, New York, New York, USA.Consortium for Advanced Science and Engineering, University of Chicago, Chicago, Illinois, USA. Computing, Environment and Life Sciences, Argonne National Laboratory, Lemont, Illinois, USA.Consortium for Advanced Science and Engineering, University of Chicago, Chicago, Illinois, USA. Computing, Environment and Life Sciences, Argonne National Laboratory, Lemont, Illinois, USA.Consortium for Advanced Science and Engineering, University of Chicago, Chicago, Illinois, USA. Computing, Environment and Life Sciences, Argonne National Laboratory, Lemont, Illinois, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, USA. Institute for Cell and Molecular Biology, The University of Texas at Austin, Austin, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA.Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, USA. Institute for Cell and Molecular Biology, The University of Texas at Austin, Austin, Texas, USA.CCDC Army Research Laboratory-South, University of Texas, Austin, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA. CCDC Army Research Laboratory-South, University of Texas, Austin, Texas, USA.Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, USA. Institute for Cell and Molecular Biology, The University of Texas at Austin, Austin, Texas, USA.Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, USA. Institute for Cell and Molecular Biology, The University of Texas at Austin, Austin, Texas, USA.Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, USA. Institute for Cell and Molecular Biology, The University of Texas at Austin, Austin, Texas, USA.Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, USA. Institute for Cell and Molecular Biology, The University of Texas at Austin, Austin, Texas, USA. Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas, USA.Center for Molecular and Translational Human Infectious Diseases Research, Department of Pathology and Genomic Medicine, Houston Methodist Research Institute, Houston Methodist Hospital, Houston, Texas, USA jmmusser@houstonmethodist.org. Department of Pathology and Laboratory Medicine, Weill Cornell Medical College, New York, New York, USA. Department of Microbiology and Immunology, Weill Cornell Medical College, New York, New York, USA.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

33127862

Citation

Long, S Wesley, et al. "Molecular Architecture of Early Dissemination and Massive Second Wave of the SARS-CoV-2 Virus in a Major Metropolitan Area." MBio, vol. 11, no. 6, 2020.
Long SW, Olsen RJ, Christensen PA, et al. Molecular Architecture of Early Dissemination and Massive Second Wave of the SARS-CoV-2 Virus in a Major Metropolitan Area. mBio. 2020;11(6).
Long, S. W., Olsen, R. J., Christensen, P. A., Bernard, D. W., Davis, J. J., Shukla, M., Nguyen, M., Saavedra, M. O., Yerramilli, P., Pruitt, L., Subedi, S., Kuo, H. C., Hendrickson, H., Eskandari, G., Nguyen, H. A. T., Long, J. H., Kumaraswami, M., Goike, J., Boutz, D., ... Musser, J. M. (2020). Molecular Architecture of Early Dissemination and Massive Second Wave of the SARS-CoV-2 Virus in a Major Metropolitan Area. MBio, 11(6). https://doi.org/10.1128/mBio.02707-20
Long SW, et al. Molecular Architecture of Early Dissemination and Massive Second Wave of the SARS-CoV-2 Virus in a Major Metropolitan Area. mBio. 2020 10 30;11(6) PubMed PMID: 33127862.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Molecular Architecture of Early Dissemination and Massive Second Wave of the SARS-CoV-2 Virus in a Major Metropolitan Area. AU - Long,S Wesley, AU - Olsen,Randall J, AU - Christensen,Paul A, AU - Bernard,David W, AU - Davis,James J, AU - Shukla,Maulik, AU - Nguyen,Marcus, AU - Saavedra,Matthew Ojeda, AU - Yerramilli,Prasanti, AU - Pruitt,Layne, AU - Subedi,Sishir, AU - Kuo,Hung-Che, AU - Hendrickson,Heather, AU - Eskandari,Ghazaleh, AU - Nguyen,Hoang A T, AU - Long,J Hunter, AU - Kumaraswami,Muthiah, AU - Goike,Jule, AU - Boutz,Daniel, AU - Gollihar,Jimmy, AU - McLellan,Jason S, AU - Chou,Chia-Wei, AU - Javanmardi,Kamyab, AU - Finkelstein,Ilya J, AU - Musser,James M, Y1 - 2020/10/30/ PY - 2020/10/31/entrez PY - 2020/11/1/pubmed PY - 2020/11/20/medline KW - COVID-19 KW - COVID-19 disease KW - SARS-CoV-2 KW - evolution KW - genome sequencing KW - molecular population genomics JF - mBio JO - mBio VL - 11 IS - 6 N2 - We sequenced the genomes of 5,085 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) strains causing two coronavirus disease 2019 (COVID-19) disease waves in metropolitan Houston, TX, an ethnically diverse region with 7 million residents. The genomes were from viruses recovered in the earliest recognized phase of the pandemic in Houston and from viruses recovered in an ongoing massive second wave of infections. The virus was originally introduced into Houston many times independently. Virtually all strains in the second wave have a Gly614 amino acid replacement in the spike protein, a polymorphism that has been linked to increased transmission and infectivity. Patients infected with the Gly614 variant strains had significantly higher virus loads in the nasopharynx on initial diagnosis. We found little evidence of a significant relationship between virus genotype and altered virulence, stressing the linkage between disease severity, underlying medical conditions, and host genetics. Some regions of the spike protein-the primary target of global vaccine efforts-are replete with amino acid replacements, perhaps indicating the action of selection. We exploited the genomic data to generate defined single amino acid replacements in the receptor binding domain of spike protein that, importantly, produced decreased recognition by the neutralizing monoclonal antibody CR3022. Our report represents the first analysis of the molecular architecture of SARS-CoV-2 in two infection waves in a major metropolitan region. The findings will help us to understand the origin, composition, and trajectory of future infection waves and the potential effect of the host immune response and therapeutic maneuvers on SARS-CoV-2 evolution.IMPORTANCE There is concern about second and subsequent waves of COVID-19 caused by the SARS-CoV-2 coronavirus occurring in communities globally that had an initial disease wave. Metropolitan Houston, TX, with a population of 7 million, is experiencing a massive second disease wave that began in late May 2020. To understand SARS-CoV-2 molecular population genomic architecture and evolution and the relationship between virus genotypes and patient features, we sequenced the genomes of 5,085 SARS-CoV-2 strains from these two waves. Our report provides the first molecular characterization of SARS-CoV-2 strains causing two distinct COVID-19 disease waves. SN - 2150-7511 UR - https://www.unboundmedicine.com/medline/citation/33127862/Molecular_Architecture_of_Early_Dissemination_and_Massive_Second_Wave_of_the_SARS_CoV_2_Virus_in_a_Major_Metropolitan_Area_ L2 - https://doi.org/10.1128/mBio.02707-20 DB - PRIME DP - Unbound Medicine ER -