Genome Sequencing of Sewage Detects Regionally Prevalent SARS-CoV-2 Variants.
Identifieur interne : 000071 ( Main/Exploration ); précédent : 000070; suivant : 000072Genome Sequencing of Sewage Detects Regionally Prevalent SARS-CoV-2 Variants.
Auteurs : Alexander Crits-Christoph [États-Unis] ; Rose S. Kantor [États-Unis] ; Matthew R. Olm [États-Unis] ; Oscar N. Whitney [États-Unis] ; Basem Al-Shayeb [États-Unis] ; Yue Clare Lou [États-Unis] ; Avi Flamholz [États-Unis] ; Lauren C. Kennedy [États-Unis] ; Hannah Greenwald [États-Unis] ; Adrian Hinkle [États-Unis] ; Jonathan Hetzel [États-Unis] ; Sara Spitzer [États-Unis] ; Jeffery Koble [États-Unis] ; Asako Tan [États-Unis] ; Fred Hyde [États-Unis] ; Gary Schroth [États-Unis] ; Scott Kuersten [États-Unis] ; Jillian F. Banfield [États-Unis] ; Kara L. Nelson [États-Unis]Source :
- mBio [ 2150-7511 ] ; 2021.
Abstract
Viral genome sequencing has guided our understanding of the spread and extent of genetic diversity of SARS-CoV-2 during the COVID-19 pandemic. SARS-CoV-2 viral genomes are usually sequenced from nasopharyngeal swabs of individual patients to track viral spread. Recently, RT-qPCR of municipal wastewater has been used to quantify the abundance of SARS-CoV-2 in several regions globally. However, metatranscriptomic sequencing of wastewater can be used to profile the viral genetic diversity across infected communities. Here, we sequenced RNA directly from sewage collected by municipal utility districts in the San Francisco Bay Area to generate complete and nearly complete SARS-CoV-2 genomes. The major consensus SARS-CoV-2 genotypes detected in the sewage were identical to clinical genomes from the region. Using a pipeline for single nucleotide variant calling in a metagenomic context, we characterized minor SARS-CoV-2 alleles in the wastewater and detected viral genotypes which were also found within clinical genomes throughout California. Observed wastewater variants were more similar to local California patient-derived genotypes than they were to those from other regions within the United States or globally. Additional variants detected in wastewater have only been identified in genomes from patients sampled outside California, indicating that wastewater sequencing can provide evidence for recent introductions of viral lineages before they are detected by local clinical sequencing. These results demonstrate that epidemiological surveillance through wastewater sequencing can aid in tracking exact viral strains in an epidemic context.
DOI: 10.1128/mBio.02703-20
PubMed: 33468686
Affiliations:
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Kantor</name><affiliation wicri:level="2"><nlm:affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Civil and Environmental Engineering, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Olm, Matthew R" sort="Olm, Matthew R" uniqKey="Olm M" first="Matthew R" last="Olm">Matthew R. Olm</name><affiliation wicri:level="4"><nlm:affiliation>Department of Microbiology and Immunology, Stanford University, Stanford, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, Stanford University, Stanford, California</wicri:regionArea><placeName><region type="state">Californie</region><settlement type="city">Stanford (Californie)</settlement></placeName><orgName type="university">Université Stanford</orgName></affiliation></author><author><name sortKey="Whitney, Oscar N" sort="Whitney, Oscar N" uniqKey="Whitney O" first="Oscar N" last="Whitney">Oscar N. Whitney</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cell Biology, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular and Cell Biology, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Al Shayeb, Basem" sort="Al Shayeb, Basem" uniqKey="Al Shayeb B" first="Basem" last="Al-Shayeb">Basem Al-Shayeb</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant and Microbial Biology, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant and Microbial Biology, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Innovative Genomics Institute, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Innovative Genomics Institute, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Lou, Yue Clare" sort="Lou, Yue Clare" uniqKey="Lou Y" first="Yue Clare" last="Lou">Yue Clare Lou</name><affiliation wicri:level="2"><nlm:affiliation>Department of Plant and Microbial Biology, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant and Microbial Biology, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Innovative Genomics Institute, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Innovative Genomics Institute, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Flamholz, Avi" sort="Flamholz, Avi" uniqKey="Flamholz A" first="Avi" last="Flamholz">Avi Flamholz</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular and Cell Biology, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular and Cell Biology, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Kennedy, Lauren C" sort="Kennedy, Lauren C" uniqKey="Kennedy L" first="Lauren C" last="Kennedy">Lauren C. Kennedy</name><affiliation wicri:level="2"><nlm:affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Civil and Environmental Engineering, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Greenwald, Hannah" sort="Greenwald, Hannah" uniqKey="Greenwald H" first="Hannah" last="Greenwald">Hannah Greenwald</name><affiliation wicri:level="2"><nlm:affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Civil and Environmental Engineering, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Hinkle, Adrian" sort="Hinkle, Adrian" uniqKey="Hinkle A" first="Adrian" last="Hinkle">Adrian Hinkle</name><affiliation wicri:level="2"><nlm:affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Civil and Environmental Engineering, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Hetzel, Jonathan" sort="Hetzel, Jonathan" uniqKey="Hetzel J" first="Jonathan" last="Hetzel">Jonathan Hetzel</name><affiliation wicri:level="2"><nlm:affiliation>Illumina, San Diego, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Illumina, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Spitzer, Sara" sort="Spitzer, Sara" uniqKey="Spitzer S" first="Sara" last="Spitzer">Sara Spitzer</name><affiliation wicri:level="2"><nlm:affiliation>Illumina, San Diego, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Illumina, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Koble, Jeffery" sort="Koble, Jeffery" uniqKey="Koble J" first="Jeffery" last="Koble">Jeffery Koble</name><affiliation wicri:level="2"><nlm:affiliation>Illumina, San Diego, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Illumina, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Tan, Asako" sort="Tan, Asako" uniqKey="Tan A" first="Asako" last="Tan">Asako Tan</name><affiliation wicri:level="2"><nlm:affiliation>Illumina, San Diego, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Illumina, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Hyde, Fred" sort="Hyde, Fred" uniqKey="Hyde F" first="Fred" last="Hyde">Fred Hyde</name><affiliation wicri:level="2"><nlm:affiliation>Illumina, Madison, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Illumina, Madison, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author><author><name sortKey="Schroth, Gary" sort="Schroth, Gary" uniqKey="Schroth G" first="Gary" last="Schroth">Gary Schroth</name><affiliation wicri:level="2"><nlm:affiliation>Illumina, San Diego, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Illumina, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Kuersten, Scott" sort="Kuersten, Scott" uniqKey="Kuersten S" first="Scott" last="Kuersten">Scott Kuersten</name><affiliation wicri:level="2"><nlm:affiliation>Illumina, Madison, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Illumina, Madison, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author><author><name sortKey="Banfield, Jillian F" sort="Banfield, Jillian F" uniqKey="Banfield J" first="Jillian F" last="Banfield">Jillian F. Banfield</name><affiliation wicri:level="2"><nlm:affiliation>Innovative Genomics Institute, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Innovative Genomics Institute, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Environmental Science, Policy, and Management, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Chan Zuckerberg Biohub, San Francisco, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Chan Zuckerberg Biohub, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Nelson, Kara L" sort="Nelson, Kara L" uniqKey="Nelson K" first="Kara L" last="Nelson">Kara L. Nelson</name><affiliation wicri:level="2"><nlm:affiliation>Innovative Genomics Institute, Berkeley, California, USA karanelson@berkeley.edu.</nlm:affiliation><country wicri:rule="url">États-Unis</country><wicri:regionArea>Innovative Genomics Institute, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Civil and Environmental Engineering, University of California, Berkeley, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2021" type="published">2021</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Viral genome sequencing has guided our understanding of the spread and extent of genetic diversity of SARS-CoV-2 during the COVID-19 pandemic. SARS-CoV-2 viral genomes are usually sequenced from nasopharyngeal swabs of individual patients to track viral spread. Recently, RT-qPCR of municipal wastewater has been used to quantify the abundance of SARS-CoV-2 in several regions globally. However, metatranscriptomic sequencing of wastewater can be used to profile the viral genetic diversity across infected communities. Here, we sequenced RNA directly from sewage collected by municipal utility districts in the San Francisco Bay Area to generate complete and nearly complete SARS-CoV-2 genomes. The major consensus SARS-CoV-2 genotypes detected in the sewage were identical to clinical genomes from the region. Using a pipeline for single nucleotide variant calling in a metagenomic context, we characterized minor SARS-CoV-2 alleles in the wastewater and detected viral genotypes which were also found within clinical genomes throughout California. Observed wastewater variants were more similar to local California patient-derived genotypes than they were to those from other regions within the United States or globally. Additional variants detected in wastewater have only been identified in genomes from patients sampled outside California, indicating that wastewater sequencing can provide evidence for recent introductions of viral lineages before they are detected by local clinical sequencing. These results demonstrate that epidemiological surveillance through wastewater sequencing can aid in tracking exact viral strains in an epidemic context.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">33468686</PMID><DateRevised><Year>2021</Year><Month>01</Month><Day>22</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN><JournalIssue CitedMedium="Internet"><Volume>12</Volume><Issue>1</Issue><PubDate><Year>2021</Year><Month>01</Month><Day>19</Day></PubDate></JournalIssue><Title>mBio</Title><ISOAbbreviation>mBio</ISOAbbreviation></Journal><ArticleTitle>Genome Sequencing of Sewage Detects Regionally Prevalent SARS-CoV-2 Variants.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e02703-20</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.02703-20</ELocationID><Abstract><AbstractText>Viral genome sequencing has guided our understanding of the spread and extent of genetic diversity of SARS-CoV-2 during the COVID-19 pandemic. SARS-CoV-2 viral genomes are usually sequenced from nasopharyngeal swabs of individual patients to track viral spread. Recently, RT-qPCR of municipal wastewater has been used to quantify the abundance of SARS-CoV-2 in several regions globally. However, metatranscriptomic sequencing of wastewater can be used to profile the viral genetic diversity across infected communities. Here, we sequenced RNA directly from sewage collected by municipal utility districts in the San Francisco Bay Area to generate complete and nearly complete SARS-CoV-2 genomes. The major consensus SARS-CoV-2 genotypes detected in the sewage were identical to clinical genomes from the region. Using a pipeline for single nucleotide variant calling in a metagenomic context, we characterized minor SARS-CoV-2 alleles in the wastewater and detected viral genotypes which were also found within clinical genomes throughout California. Observed wastewater variants were more similar to local California patient-derived genotypes than they were to those from other regions within the United States or globally. Additional variants detected in wastewater have only been identified in genomes from patients sampled outside California, indicating that wastewater sequencing can provide evidence for recent introductions of viral lineages before they are detected by local clinical sequencing. These results demonstrate that epidemiological surveillance through wastewater sequencing can aid in tracking exact viral strains in an epidemic context.</AbstractText><CopyrightInformation>Copyright © 2021 Crits-Christoph et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Crits-Christoph</LastName><ForeName>Alexander</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Plant and Microbial Biology, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Innovative Genomics Institute, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kantor</LastName><ForeName>Rose S</ForeName><Initials>RS</Initials><AffiliationInfo><Affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Olm</LastName><ForeName>Matthew R</ForeName><Initials>MR</Initials><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, Stanford University, Stanford, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Whitney</LastName><ForeName>Oscar N</ForeName><Initials>ON</Initials><AffiliationInfo><Affiliation>Department of Molecular and Cell Biology, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Al-Shayeb</LastName><ForeName>Basem</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Department of Plant and Microbial Biology, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Innovative Genomics Institute, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lou</LastName><ForeName>Yue Clare</ForeName><Initials>YC</Initials><AffiliationInfo><Affiliation>Department of Plant and Microbial Biology, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Innovative Genomics Institute, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Flamholz</LastName><ForeName>Avi</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Molecular and Cell Biology, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kennedy</LastName><ForeName>Lauren C</ForeName><Initials>LC</Initials><AffiliationInfo><Affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Greenwald</LastName><ForeName>Hannah</ForeName><Initials>H</Initials><AffiliationInfo><Affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hinkle</LastName><ForeName>Adrian</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hetzel</LastName><ForeName>Jonathan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Illumina, San Diego, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Spitzer</LastName><ForeName>Sara</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Illumina, San Diego, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Koble</LastName><ForeName>Jeffery</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Illumina, San Diego, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tan</LastName><ForeName>Asako</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Illumina, San Diego, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hyde</LastName><ForeName>Fred</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Illumina, Madison, Wisconsin, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schroth</LastName><ForeName>Gary</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Illumina, San Diego, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kuersten</LastName><ForeName>Scott</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Illumina, Madison, Wisconsin, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Banfield</LastName><ForeName>Jillian F</ForeName><Initials>JF</Initials><AffiliationInfo><Affiliation>Innovative Genomics Institute, Berkeley, California, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Chan Zuckerberg Biohub, San Francisco, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nelson</LastName><ForeName>Kara L</ForeName><Initials>KL</Initials><AffiliationInfo><Affiliation>Innovative Genomics Institute, Berkeley, California, USA karanelson@berkeley.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Civil and Environmental Engineering, University of California, Berkeley, California, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2021</Year><Month>01</Month><Day>19</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mBio</MedlineTA><NlmUniqueID>101519231</NlmUniqueID></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">coronavirus</Keyword><Keyword MajorTopicYN="Y">environmental microbiology</Keyword><Keyword MajorTopicYN="Y">genomics</Keyword><Keyword MajorTopicYN="Y">metagenomics</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2021</Year><Month>1</Month><Day>20</Day><Hour>5</Hour><Minute>44</Minute></PubMedPubDate><PubMedPubDate 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Nat Methods. 2020;17:261–272.</Citation><ArticleIdList><ArticleId IdType="doi">10.1038/s41592-019-0686-2</ArticleId></ArticleIdList></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>États-Unis</li></country><region><li>Californie</li><li>Wisconsin</li></region><settlement><li>Stanford (Californie)</li></settlement><orgName><li>Université Stanford</li></orgName></list><tree><country name="États-Unis"><region name="Californie"><name sortKey="Crits Christoph, Alexander" sort="Crits Christoph, Alexander" uniqKey="Crits Christoph A" first="Alexander" last="Crits-Christoph">Alexander Crits-Christoph</name></region><name sortKey="Al Shayeb, Basem" sort="Al Shayeb, Basem" uniqKey="Al Shayeb B" first="Basem" last="Al-Shayeb">Basem Al-Shayeb</name><name sortKey="Al Shayeb, Basem" sort="Al Shayeb, Basem" uniqKey="Al Shayeb B" first="Basem" last="Al-Shayeb">Basem Al-Shayeb</name><name sortKey="Banfield, Jillian F" sort="Banfield, Jillian F" uniqKey="Banfield J" first="Jillian F" last="Banfield">Jillian F. Banfield</name><name sortKey="Banfield, Jillian F" sort="Banfield, Jillian F" uniqKey="Banfield J" first="Jillian F" last="Banfield">Jillian F. Banfield</name><name sortKey="Banfield, Jillian F" sort="Banfield, Jillian F" uniqKey="Banfield J" first="Jillian F" last="Banfield">Jillian F. Banfield</name><name sortKey="Banfield, Jillian F" sort="Banfield, Jillian F" uniqKey="Banfield J" first="Jillian F" last="Banfield">Jillian F. 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Olm</name><name sortKey="Schroth, Gary" sort="Schroth, Gary" uniqKey="Schroth G" first="Gary" last="Schroth">Gary Schroth</name><name sortKey="Spitzer, Sara" sort="Spitzer, Sara" uniqKey="Spitzer S" first="Sara" last="Spitzer">Sara Spitzer</name><name sortKey="Tan, Asako" sort="Tan, Asako" uniqKey="Tan A" first="Asako" last="Tan">Asako Tan</name><name sortKey="Whitney, Oscar N" sort="Whitney, Oscar N" uniqKey="Whitney O" first="Oscar N" last="Whitney">Oscar N. Whitney</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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