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Editor's Pick Research Article | Ecological and Evolutionary Science

Discovery and Genomic Characterization of a 382-Nucleotide Deletion in ORF7b and ORF8 during the Early Evolution of SARS-CoV-2

Yvonne C. F. Su, Danielle E. Anderson, Barnaby E. Young, Martin Linster, Feng Zhu, Jayanthi Jayakumar, Yan Zhuang, Shirin Kalimuddin, Jenny G. H. Low, Chee Wah Tan, Wan Ni Chia, Tze Minn Mak, Sophie Octavia, Jean-Marc Chavatte, Raphael T. C. Lee, Surinder Pada, Seow Yen Tan, Louisa Sun, Gabriel Z. Yan, Sebastian Maurer-Stroh, Ian H. Mendenhall, Yee-Sin Leo, David Chien Lye, Lin-Fa Wang, Gavin J. D. Smith
Stacey Schultz-Cherry, Editor
Yvonne C. F. Su
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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  • ORCID record for Yvonne C. F. Su
Danielle E. Anderson
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Barnaby E. Young
bNational Centre for Infectious Diseases, Singapore
cTan Tock Seng Hospital, Singapore
dLee Kong Chian School of Medicine, Singapore
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Martin Linster
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Feng Zhu
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Jayanthi Jayakumar
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Yan Zhuang
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Shirin Kalimuddin
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
eSingapore General Hospital, Singapore
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  • ORCID record for Shirin Kalimuddin
Jenny G. H. Low
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
eSingapore General Hospital, Singapore
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  • ORCID record for Jenny G. H. Low
Chee Wah Tan
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Wan Ni Chia
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
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Tze Minn Mak
bNational Centre for Infectious Diseases, Singapore
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Sophie Octavia
bNational Centre for Infectious Diseases, Singapore
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Jean-Marc Chavatte
bNational Centre for Infectious Diseases, Singapore
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Raphael T. C. Lee
fBioinformatics Institute, Agency for Science, Technology and Research (A*STAR), Singapore
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Surinder Pada
gNg Teng Fong General Hospital, Singapore
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Seow Yen Tan
hChangi General Hospital, Singapore
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Louisa Sun
iAlexandra Hospital, Singapore
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Gabriel Z. Yan
jNational University Hospital, Singapore
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Sebastian Maurer-Stroh
fBioinformatics Institute, Agency for Science, Technology and Research (A*STAR), Singapore
kDepartment of Biological Sciences, National University of Singapore, Singapore
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Ian H. Mendenhall
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
mSingHealth Duke-NUS Global Health Institute, Singapore
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Yee-Sin Leo
bNational Centre for Infectious Diseases, Singapore
cTan Tock Seng Hospital, Singapore
dLee Kong Chian School of Medicine, Singapore
lSaw Swee Hock School of Public Health, National University of Singapore, Singapore
nYong Loo Lin School of Medicine, National University of Singapore, Singapore
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David Chien Lye
bNational Centre for Infectious Diseases, Singapore
cTan Tock Seng Hospital, Singapore
dLee Kong Chian School of Medicine, Singapore
nYong Loo Lin School of Medicine, National University of Singapore, Singapore
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Lin-Fa Wang
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
mSingHealth Duke-NUS Global Health Institute, Singapore
oDuke Global Health Institute, Duke University, North Carolina, USA
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Gavin J. D. Smith
aProgramme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore
mSingHealth Duke-NUS Global Health Institute, Singapore
oDuke Global Health Institute, Duke University, North Carolina, USA
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Stacey Schultz-Cherry
St. Jude Children's Research Hospital
Roles: Editor
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DOI: 10.1128/mBio.01610-20
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    FIG 1

    Genomic organization and evolutionary relationships of human SARS-CoV-2 and SARS-CoV-2 Δ382. (A) Schematic diagram of the genomes of SARS-CoV-2 isolates Wuhan-Hu-1 (GenBank accession no. MN908947) and human CoV-19/Singapore/12/2020 (hCoV-19/Singapore/12/2020) Δ382 (GISAID: EPI_ISL_414378). (B) Magnification of genomic region (pink box in panel A) showing the 382-nt deletion in ORF7b and ORF8 (indicated by red line) in hCoV-19/Singapore/12/2020. Other ORF7b/8 deletions are indicated by blue lines as follows: a 138-nt deletion in hCoV-19/Australia/VIC671/2020 (EPI_ISL_426967), a 345-nt deletion in hCoV-19/Bangladesh/BARJ_CVASU_CTG_517/2020 (EPI_ISL_450344), and a 62-nt deletion in hCoV-19/Spain/COV001404/2020 (EPI_ISL_452497). Horizontal axes indicate the nucleotide position relative to Wuhan-Hu-1; open reading frames (ORFs) are indicated by solid colored arrows. Transcription regulatory sequences (TRSs) are indicated by yellow arrows. (C) Temporal phylogeny of 419 complete genomes inferred using an uncorrelated lognormal relaxed clock model in BEAST. Colored circles at the tips represent geographic locations of virus sampling. Colored triangles represent ORF7b/8 deletion variants. A fully labeled tree with Bayesian posterior probabilities indicated is presented in Fig. S4. Red isolate names indicate SARS-CoV-2 from Singapore with a 382-nt deletion as described in this study. Blue isolate names indicate a 382-nt deletion from Taiwan, whereas green isolate names indicate a 138-nt deletion from Australia. Node A represents the time to most common ancestor (TMRCA) for the lineage containing Δ382 viruses from Singapore and Taiwan, while node B represents the TMRCA of the clade containing Δ382 viruses from Singapore. Bayesian posterior probabilities of ≥0.95 are indicated at nodes. Scale bar represents time in years. Abbreviations: AUS, Australia; SP, Spain; BGD, Bangladesh.

  • FIG 2
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    FIG 2

    Prevalence, viral antigen staining, and growth kinetics of human SARS-CoV-2 and SARS-CoV-2 Δ382. (A) Daily number of wild-type and Δ382 deletion variants of SARS-CoV-2 detected in Singapore based on PCR screening of 191 patient specimens. (B) Cellular and viral fluorescence staining of SARS-CoV-2 wild-type and Δ382 strains in Vero-E6 cells. Bright-field images were captured to visualize cytopathic effect. SARS-CoV-2 antigen was stained with COVID-19 convalescent-phase serum. Red, viral proteins; blue, DAPI (nuclei). (C) Growth curves of SARS-CoV-2 wild-type and Δ382 strains at a multiplicity of infection (MOI) of 0.01 in Vero-E6 cells. Virus titers were expressed as 50% tissue culture infectious doses (TCID50)/ml and were plotted as means of results from three independent replicates and standard deviations. Error bars indicate standard errors of means. Significance was calculated by two-way ANOVA with Tukey’s multiple-comparison test.

Supplemental Material

  • Figures
  • FIG S1

    Sanger sequences of hCoV-19/Singapore/12/2020 Δ382 mapped to Wuhan-Hu-1 showing the position of the 382-nt deletion in the ORF7b and ORF8 regions of the SARS-CoV-2 genome. Download FIG S1, PDF file, 0.7 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S2

    Amino acid sequences of the ORF7b region in SARS-CoV-2 and SARS-CoV-2 Δ382. Truncated ORF7b is observed as a result of the deleted C terminus of ORF7b in SARS-CoV-2 Δ382. Download FIG S2, PDF file, 0.4 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S1

    List of specimens from which full genomes were generated. Download Table S1, DOCX file, 0.01 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S3

    Maximum-likelihood tree of SARS-CoV-2 genomes (n = 1,038) reconstructed using RAxML with bootstrap values of >50 indicated at branch nodes. Download FIG S3, PDF file, 0.3 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S4

    Evolutionary relationships of human SARS-CoV-2 and SARS-CoV-2 Δ382. Temporal phylogeny of 419 complete genomes was inferred using an uncorrelated lognormal relaxed clock model in BEAST. Colored virus names represent different geographic locations. Bayesian posterior probabilities of ≥0.95 are indicated at nodes. The scale bar represents time in years. Download FIG S4, PDF file, 0.3 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2

    Comparison of genome similarities between SARS-CoV-2 Δ382 viruses and the wild-type virus Wuhan-Hu-1 SARS-CoV-2. Download Table S2, DOCX file, 0.01 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S3

    Estimated dates of nodes within the SARS-CoV-2 phylogeny shown in Fig. 1C. Download Table S3, DOCX file, 0.01 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S4

    Summary of deletion variants of SARS-CoV-2. Download Table S4, DOCX file, 0.01 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • FIG S5

    Comparison of data representing transcription of different SARS-CoV-2 genes in wild-type (WT) versus Δ382 viruses. The abundance of mapped reads relative to transcription regulatory sequence (TRS) positions across the genome was determined. Transcripts per million (TPM) reads were calculated from reads mapped specifically to each leader-TRS region, and a whisker and a scatter plot was drawn for each gene. A Wilcoxon test was applied to the TPM data for comparison of each gene of Δ382 to the WT (*, P ≤ 0.05; **, P ≤ 0.01). Download FIG S5, PDF file, 0.2 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S5

    Viruses included in phylogenetic analyses. Download Table S5, PDF file, 0.1 MB.

    Copyright © 2020 Su et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Discovery and Genomic Characterization of a 382-Nucleotide Deletion in ORF7b and ORF8 during the Early Evolution of SARS-CoV-2
Yvonne C. F. Su, Danielle E. Anderson, Barnaby E. Young, Martin Linster, Feng Zhu, Jayanthi Jayakumar, Yan Zhuang, Shirin Kalimuddin, Jenny G. H. Low, Chee Wah Tan, Wan Ni Chia, Tze Minn Mak, Sophie Octavia, Jean-Marc Chavatte, Raphael T. C. Lee, Surinder Pada, Seow Yen Tan, Louisa Sun, Gabriel Z. Yan, Sebastian Maurer-Stroh, Ian H. Mendenhall, Yee-Sin Leo, David Chien Lye, Lin-Fa Wang, Gavin J. D. Smith
mBio Jul 2020, 11 (4) e01610-20; DOI: 10.1128/mBio.01610-20

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Discovery and Genomic Characterization of a 382-Nucleotide Deletion in ORF7b and ORF8 during the Early Evolution of SARS-CoV-2
Yvonne C. F. Su, Danielle E. Anderson, Barnaby E. Young, Martin Linster, Feng Zhu, Jayanthi Jayakumar, Yan Zhuang, Shirin Kalimuddin, Jenny G. H. Low, Chee Wah Tan, Wan Ni Chia, Tze Minn Mak, Sophie Octavia, Jean-Marc Chavatte, Raphael T. C. Lee, Surinder Pada, Seow Yen Tan, Louisa Sun, Gabriel Z. Yan, Sebastian Maurer-Stroh, Ian H. Mendenhall, Yee-Sin Leo, David Chien Lye, Lin-Fa Wang, Gavin J. D. Smith
mBio Jul 2020, 11 (4) e01610-20; DOI: 10.1128/mBio.01610-20
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KEYWORDS

COVID-19
ORF8
natural selection
phylogeny
vaccines

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