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. 2020 Jul 31;369(6503):582-587.
doi: 10.1126/science.abb9263. Epub 2020 Jun 8.

Genomic surveillance reveals multiple introductions of SARS-CoV-2 into Northern California

Xianding Deng #  1   2 , Wei Gu #  1   2 , Scot Federman #  1   2 , Louis du Plessis #  3 , Oliver G Pybus  3   4 , Nuno R Faria  3   5 , Candace Wang  1   2 , Guixia Yu  1   2 , Brian Bushnell  6 , Chao-Yang Pan  7 , Hugo Guevara  7 , Alicia Sotomayor-Gonzalez  1   2 , Kelsey Zorn  8 , Allan Gopez  1 , Venice Servellita  1 , Elaine Hsu  1 , Steve Miller  1 , Trevor Bedford  9   10 , Alexander L Greninger  9   11 , Pavitra Roychoudhury  9   11 , Lea M Starita  10   12 , Michael Famulare  13 , Helen Y Chu  10   14 , Jay Shendure  10   11   15 , Keith R Jerome  9   11 , Catie Anderson  16 , Karthik Gangavarapu  16 , Mark Zeller  16 , Emily Spencer  16 , Kristian G Andersen  16 , Duncan MacCannell  17 , Clinton R Paden  17 , Yan Li  17 , Jing Zhang  17 , Suxiang Tong  17 , Gregory Armstrong  17 , Scott Morrow  18 , Matthew Willis  19 , Bela T Matyas  20 , Sundari Mase  21 , Olivia Kasirye  22 , Maggie Park  23 , Godfred Masinde  24 , Curtis Chan  24 , Alexander T Yu  7 , Shua J Chai  7   17 , Elsa Villarino  25 , Brandon Bonin  25 , Debra A Wadford  7 , Charles Y Chiu  26   2   27
Affiliations

Genomic surveillance reveals multiple introductions of SARS-CoV-2 into Northern California

Xianding Deng et al. Science. .

Abstract

The coronavirus disease 2019 (COVID-19) pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has spread globally, with >365,000 cases in California as of 17 July 2020. We investigated the genomic epidemiology of SARS-CoV-2 in Northern California from late January to mid-March 2020, using samples from 36 patients spanning nine counties and the Grand Princess cruise ship. Phylogenetic analyses revealed the cryptic introduction of at least seven different SARS-CoV-2 lineages into California, including epidemic WA1 strains associated with Washington state, with lack of a predominant lineage and limited transmission among communities. Lineages associated with outbreak clusters in two counties were defined by a single base substitution in the viral genome. These findings support contact tracing, social distancing, and travel restrictions to contain the spread of SARS-CoV-2 in California and other states.

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Figures

Fig. 1
Fig. 1. Genomic survey of SARS-CoV-2 genomes in Northern California.
(A) Analysis workflow. (B) Map of the Northern California survey region divided by county. The pie charts for each county are subdivided according to the number of patients whose viral genome was sequenced, and the color corresponds to the viral lineage as determined by phylogenetic analysis. Passengers (n = 3) who were on the Grand Princess cruise ship during voyage A to Mexico and disembarked to return to their home communities are denoted by a ship icon facing left, while passengers (n = 8) aboard the Grand Princess cruise ship during voyage B to Hawaii are denoted by a ship icon facing right. Abbreviations: SCCPHD, Santa Clara County Public Health Department; CDPH, California Department of Public Health; UCSF, University of California San Francisco; MSSPE, Metagenomic Sequencing with Spiked Primer Enrichment; NGS, next-generation sequencing.
Fig. 2
Fig. 2. Phylogeny of SARS-CoV-2 lineages in California.
(A) Phylogenetic tree of 753 SARS-CoV-2 genomes from GISAID (till Mar 20, 2020) along with the 36 genomes in this survey (tree file attached in supplementary material). Genomes from Northern California sequenced in the current study are denoted with colored circles, while other genomes sequenced from California and from other states in the US are denoted with black and gray circles, respectively. The name of each lineage or outbreak cluster is shown next to the arc line. (B) Phylogenetic subtree corresponding to the WA1 lineage. This subtree was reconstructed from 88 SARS-CoV-2 genomes after removal of ambiguous nucleotide sites that had generated low-coverage artifacts (see text). The WA1 virus from Washington state (first case in the US) is at the root of the subtree along with a virus sequenced in China. The UC19 virus (from a Grand Princess voyage A passenger) is basal to the viruses sequenced from crew members and passengers on voyage B. (C) Zoomed view of the SCC1 lineage associated with the Santa Clara County outbreak cluster. (D) Zoomed view of the Solano County cluster. The x-axis shows the number of base substitutions relative to the root of the phylogenetic tree. The key SNVs defining a lineage or cluster are shown in red text. Bootstrap values (converted from the approximate likelihood ratio test, or aLRT score) are displayed at each node, with a value of 1 indicating 100% support.
Fig. 3
Fig. 3. Multiple sequence alignment of all SARS-CoV-2 genomes reported across 9 Northern California counties and the Grand Princess cruise ship.
Single nucleotide variants (SNVs) with respect to the reference genome (NC_045512) are shown as vertical red and black lines for lineage defining SNVs and other SNVs, respectively. Cases that are part of the WA1 lineage include the first case of COVID-19 infection (WA1) in the US, 8 passengers and crew members aboard the Grand Princess cruise ship during its second trip (voyage B), and 3 individuals surveyed from 3 Northern California counties as passengers on the ship’s first trip (voyage A). The three SNVs C8782T, C18060T, and T28144C define the WA1 lineage, and the two SNVs C17747T, A17858G are common to Grand Princess passengers and crew. Viruses from voyage B passengers and crew share SNVs G16975T and C23185T that are lacking in viruses from voyage A passengers. Single SNV variants C9924T and G29711T define the lineages from Solano County and Santa Clara County, respectively. The putative epidemiological link and sample collection date are shown beside the sequence alignment.
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