{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T15:24:27Z","timestamp":1791559467734,"version":"4.3.4"},"reference-count":57,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,9,10]],"date-time":"2021-09-10T00:00:00Z","timestamp":1631232000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000691","name":"Academy of Medical Sciences","doi-asserted-by":"publisher","award":["SGL016_1086"],"award-info":[{"award-number":["SGL016_1086"]}],"id":[{"id":"10.13039\/501100000691","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000848","name":"University of Edinburgh","doi-asserted-by":"publisher","award":["J22738"],"award-info":[{"award-number":["J22738"]}],"id":[{"id":"10.13039\/501100000848","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    <jats:bold>Background:<\/jats:bold>\n                    Hospital wastewater is a major source of antimicrobial resistance (AMR) outflow into the environment. This study uses metagenomics to study how hospital clinical activity impacts antimicrobial resistance genes (ARGs) abundances in hospital wastewater.\n                  <\/jats:p>\n                  <jats:p>\n                    <jats:bold>Methods:<\/jats:bold>\n                    Sewage was collected over a 24-h period from multiple wastewater collection points (CPs) representing different specialties within a tertiary hospital site and simultaneously from community sewage works. High throughput shotgun sequencing was performed using Illumina HiSeq4000. ARG abundances were correlated to hospital antimicrobial usage (AMU), data on clinical activity and resistance prevalence in clinical isolates.\n                  <\/jats:p>\n                  <jats:p>\n                    <jats:bold>Results:<\/jats:bold>\n                    Microbiota and ARG composition varied between CPs and overall ARG abundance was higher in hospital wastewater than in community influent. ARG and microbiota compositions were correlated (Procrustes analysis,\n                    <jats:italic>p<\/jats:italic>\n                    =0.014). Total antimicrobial usage was not associated with higher ARG abundance in wastewater. However, there was a small positive association between resistance genes and antimicrobial usage matched to ARG phenotype (IRR 1.11, CI 1.06\u20131.16,\n                    <jats:italic>p<\/jats:italic>\n                    &amp;lt;0.001). Furthermore, analyzing carbapenem and vancomycin resistance separately indicated that counts of ARGs to these antimicrobials were positively associated with their increased usage [carbapenem rate ratio (RR) 1.91, 95% CI 1.01\u20133.72,\n                    <jats:italic>p<\/jats:italic>\n                    =0.07, and vancomycin RR 10.25, CI 2.32\u201349.10,\n                    <jats:italic>p<\/jats:italic>\n                    &amp;lt;0.01]. Overall, ARG abundance within hospital wastewater did not reflect resistance patterns in clinical isolates from concurrent hospital inpatients. However, for clinical isolates of the family\n                    <jats:italic>Enterococcaceae<\/jats:italic>\n                    and\n                    <jats:italic>Staphylococcaceae<\/jats:italic>\n                    , there was a positive relationship with wastewater ARG abundance [odds ratio (OR) 1.62, CI 1.33\u20132.00,\n                    <jats:italic>p<\/jats:italic>\n                    &amp;lt;0.001, and OR 1.65, CI 1.21\u20132.30,\n                    <jats:italic>p<\/jats:italic>\n                    =0.006 respectively].\n                  <\/jats:p>\n                  <jats:p>\n                    <jats:bold>Conclusion:<\/jats:bold>\n                    We found that the relationship between hospital wastewater ARGs and antimicrobial usage or clinical isolate resistance varies by specific antimicrobial and bacterial family studied. One explanation, we consider is that relationships observed from multiple departments within a single hospital site will be detectable only for ARGs against parenteral antimicrobials uniquely used in the hospital setting. Our work highlights that using metagenomics to identify the full range of ARGs in hospital wastewater is a useful surveillance tool to monitor hospital ARG carriage and outflow and guide environmental policy on AMR.\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2021.703560","type":"journal-article","created":{"date-parts":[[2021,9,10]],"date-time":"2021-09-10T01:27:11Z","timestamp":1631237231000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":76,"title":["Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family"],"prefix":"10.3389","volume":"12","author":[{"given":"Meghan R.","family":"Perry","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hannah C.","family":"Lepper","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Luke","family":"McNally","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bryan A.","family":"Wee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick","family":"Munk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amanda","family":"Warr","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara","family":"Moore","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pota","family":"Kalima","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carol","family":"Philip","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Maria","family":"de Roda Husman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frank M.","family":"Aarestrup","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark E. J.","family":"Woolhouse","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bram A. D.","family":"van Bunnik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,9,10]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"630","DOI":"10.1126\/science.aba3432","article-title":"Using sewage for surveillance of antimicrobial resistance","volume":"367","author":"Aarestrup","year":"2020","journal-title":"Science"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1016\/j.talanta.2014.09.022","article-title":"The analysis of animal faeces as a tool to monitor antibiotic usage","volume":"132","author":"Berendsen","year":"2015","journal-title":"Talanta"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"105796","DOI":"10.1016\/j.envint.2020.105796","article-title":"Retrospective analysis of the global antibiotic residues that exceed the predicted no effect concentration for antimicrobial resistance in various environmental matrices","volume":"141","author":"Booth","year":"2020","journal-title":"Environ. Int."},{"key":"ref4","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/978-3-319-71404-2_5","article-title":"Unconstrained ordination,","volume-title":"Numerical Ecology With R Use R!","author":"Borcard","year":"2018"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"fiy087","DOI":"10.1093\/femsec\/fiy087","article-title":"Limited influence of hospital wastewater on the microbiome and resistome of wastewater in a community sewerage system","volume":"94","author":"Buelow","year":"2018","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref6","doi-asserted-by":"publisher","DOI":"10.1093\/femsec\/fiy101","article-title":"Water and sanitation: an essential battlefront in the war on antimicrobial resistance","volume":"94","author":"B\u00fcrgmann","year":"2018","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1135","DOI":"10.1073\/pnas.1616248114","article-title":"Multi-institute analysis of carbapenem resistance reveals remarkable diversity, unexplained mechanisms, and limited clonal outbreaks","volume":"114","author":"Cerqueira","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref8","doi-asserted-by":"publisher","DOI":"10.20944\/preprints202010.0267.v1","article-title":"Wastewater surveillance of antimicrobial resistance in human populations: a aystematic review.","author":"Chau","year":"2020"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1186\/s12859-018-2336-6","article-title":"Rapid and precise alignment of raw reads against redundant databases with KMA","volume":"19","author":"Clausen","year":"2018","journal-title":"BMC Bioinformatics"},{"key":"ref10","author":"Dabdoub","year":"2019"},{"key":"ref11","article-title":"Tackling Antimicobiral Resistance 2019\u20132024: The UK\u2019s Five-Year National Action Plan.","year":"2019"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13756-016-0108-5","article-title":"Quantitative evaluation of extended spectrum \u03b2-lactamase-producing Escherichia coli strains in the wastewater of a French teaching hospital and relation to patient strain","volume":"5","author":"Drieux","year":"2016","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"110612","DOI":"10.1016\/j.ecoenv.2020.110612","article-title":"Environmental resistome risks of wastewaters and aquatic environments deciphered by shotgun metagenomic assembly","volume":"197","author":"Ekwanzala","year":"2020","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref14","article-title":"Antimicrobial resistance in the EU\/EEA (EARS-Net): Annual Epidemiological Report 2019.","year":"2020"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13756-018-0423-0","article-title":"Extended spectrum beta-lactamase mediated resistance in carriage and clinical gram-negative ESKAPE bacteria: a comparative study between a district and tertiary hospital in South Africa","volume":"7","author":"Founou","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"626","DOI":"10.1101\/gr.232629.117","article-title":"Detection of vancomycin-resistant Enterococcus faecium hospital-adapted lineages in municipal wastewater treatment plants indicates widespread distribution and release into the environment","volume":"29","author":"Gouliouris","year":"2019","journal-title":"Genome Res."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1093\/cid\/cir202","article-title":"Carbapenem-resistant enterobacteriaceae: epidemiology and prevention","volume":"53","author":"Gupta","year":"2011","journal-title":"Clin. Infect. Dis."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"e616","DOI":"10.7717\/peerj.616","article-title":"Using observation-level randomeffects to model overdispersion in count data in ecology and evolution","volume":"2","author":"Harrison","year":"2014","journal-title":"PeerJ"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"1124","DOI":"10.1038\/s41467-019-08853-3","article-title":"Global monitoring of antimicrobial resistance based on metagenomics analyses of urban sewage","volume":"10","author":"Hendriksen","year":"2019","journal-title":"Nat. Commun."},{"key":"ref20","article-title":"NIH Human Microbiome Project-Tools and Technology.","year":"2021"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.2807\/1560-7917.ES.2019.24.37.1800497","article-title":"Population-level surveillance of antibiotic resistance in Escherichia coli through sewage analysis","volume":"24","author":"Hutinel","year":"2019","journal-title":"Euro Surveill."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1038\/s41396-018-0277-8","article-title":"Wastewater treatment plant resistomes are shaped by bacterial composition, genetic exchange, and upregulated expression in the effluent microbiomes","volume":"13","author":"Ju","year":"2019","journal-title":"ISME J."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"e00095","DOI":"10.1128\/msystems.00095-16","article-title":"Impact of sample type and DNA isolation procedure on genomic inference of microbiome composition","volume":"1","author":"Knudsen","year":"2016","journal-title":"mSystems"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"e03327","DOI":"10.1128\/AEM.03327-16","article-title":"Spread from the sink to the patient: in situ study using green fluorescent (GFP)-expressing Escherichia coli to model bacterial dispersion from hand-washing sink-trap reservoirs","volume":"83","author":"Kotay","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.envint.2018.04.029","article-title":"Selective concentration for ciprofloxacin resistance in Escherichia coli grown in complex aquatic bacterial biofilms","volume":"116","author":"Kraupner","year":"2018","journal-title":"Environ. Int."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"110487","DOI":"10.1016\/j.envres.2020.110487","article-title":"Extended-spectrum beta-lactamase-producing Escherichia coli and antimicrobial resistance in municipal and hospital wastewaters in Czech Republic: culture-based and metagenomic approaches","volume":"193","author":"Kutilova","year":"2021","journal-title":"Environ. Res."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"874","DOI":"10.1126\/science.aaf9286","article-title":"Achieving global targets for antimicrobial resistance","volume":"353","author":"Laxminarayan","year":"2016","journal-title":"Science"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"e000114","DOI":"10.1099\/mgen.0.000114","article-title":"Sharing of carbapenemase-encoding plasmids between enterobacteriaceae in UK sewage uncovered by MinION sequencing","volume":"3","author":"Ludden","year":"2017","journal-title":"Microb. Genom."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1016\/j.jgar.2016.01.008","article-title":"Emergence of ciprofloxacin-resistant extended-spectrum beta-lactamase-producing enteric bacteria in hospital wastewater and clinical sources","volume":"5","author":"Maheshwari","year":"2016","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"532","DOI":"10.1111\/jcpt.12432","article-title":"Correlation between antimicrobial resistance and antimicrobial resistance of Pseudomonas aeruginosa in a hospital setting: a 10-year study","volume":"41","author":"Mladenovic-Antic","year":"2016","journal-title":"J. Clin. Pharm. Ther."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"275","DOI":"10.2165\/00003088-199528040-00002","article-title":"Meropenem clinical pharmacokinetics","volume":"28","author":"Mouton","year":"1995","journal-title":"Clin. Pharmacokinet."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1038\/s41564-018-0192-9","article-title":"Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries","volume":"3","author":"Munk","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref33","article-title":"STARAMR.","year":"2021"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1016\/j.envpol.2016.04.033","article-title":"Ciprofloxacin residue and antibiotic-resistant biofilm bacteria in hospital effluent","volume":"214","author":"Ory","year":"2016","journal-title":"Environ. Pollut."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1016\/j.watres.2019.05.102","article-title":"Diversity and antibiotic resistance among Escherichia coli populations in hospital and community wastewater compared to wastewater at the receiving urban treatment plant","volume":"161","author":"Paulshus","year":"2019","journal-title":"Water Res."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1038\/nature17672","article-title":"Interconnected microbiomes and resistomes in low-income human habitats","volume":"533","author":"Pehrsson","year":"2016","journal-title":"Nature"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"153","DOI":"10.3389\/fmicb.2020.00153","article-title":"Microbial and viral communities and their antibiotic resistance genes throughout a hospital wastewater treatment system","volume":"11","author":"Petrovich","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1389","DOI":"10.1086\/523280","article-title":"Relationship between rates of antimicrobial consumption and the incidence of antimicrobial resistance in Staphylococcus aureus and Pseudomonas aeruginosa isolates from 47 French hospitals","volume":"28","author":"Rogues","year":"2007","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"1617","DOI":"10.1093\/jac\/dkx017","article-title":"Overexpression of antibiotic resistance genes in hospital effluents over time","volume":"72","author":"Rowe","year":"2017","journal-title":"J. Antimicrob. Chemother."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"834","DOI":"10.7326\/0003-4819-136-11-200206040-00013","article-title":"The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, enterococcus, gram-negative bacilli, clostridium difficile, and candida","volume":"136","author":"Safdar","year":"2002","journal-title":"Ann. Intern. Med."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1080\/09603123.2012.678000","article-title":"Decreased aztreonam susceptibility among Pseudomonas aeruginosa isolates from hospital effluent treatment system and clinical samples","volume":"22","author":"Santoro","year":"2012","journal-title":"Int. J. Environ. Health Res."},{"key":"ref42","article-title":"Human Sequence Removal. National Center for Biotechnology Information.","author":"Sherry","year":"2011"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1128","DOI":"10.1126\/science.1176950","article-title":"Functional characterization of the antibiotic resistance reservoir in the human microflora","volume":"325","author":"Sommer","year":"2009","journal-title":"Science"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.ijantimicag.2016.04.028","article-title":"Metagenomic analysis reveals that bacteriophages are reservoirs of antibiotic resistance genes","volume":"48","author":"Subirats","year":"2016","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"1350","DOI":"10.1128\/AEM.02254-07","article-title":"Molecular structure and transferability of Tn1546-like elements in Enterococcus faecium isolates from clinical, sewage, and surface water samples in Iran","volume":"74","author":"Talebi","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/S1473-3099(18)30060-4","article-title":"WHO global antimicrobial resistance surveillance system early implementation 2016-17","volume":"18","author":"Tornimbene","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1016\/j.ijheh.2007.02.010","article-title":"Are antibiotic-resistant Pseudomonas aeruginosa isolated from hospitalised patients recovered in the hospital effluents?","volume":"211","author":"Tum\u00e9o","year":"2008","journal-title":"Int. J. Hyg. Environ. Health"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"55","DOI":"10.3389\/fpubh.2020.00055","article-title":"Gastrointestinal carriage of vancomycin-resistant enterococci and carbapenem-resistant gram-negative bacteria in an endemic setting: prevalence, risk factors, and outcomes","volume":"8","author":"Vasilakopoulou","year":"2020","journal-title":"Front. Public Health"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"e619","DOI":"10.1016\/S2214-109X(18)30186-4","article-title":"Antimicrobial consumption and resistance in adult hospital inpatients in 53 countries: results of an internet-based global point prevalence survey","volume":"6","author":"Versporten","year":"2018","journal-title":"Lancet Glob. Health"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/S1473-3099(12)70317-1","article-title":"The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria","volume":"13","author":"Wellington","year":"2013","journal-title":"Lancet Infect. Dis."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"R46","DOI":"10.1186\/gb-2014-15-3-r46","article-title":"Kraken: ultrafast metagenomic sequence classification using exact alignments","volume":"15","author":"Wood","year":"2014","journal-title":"Genome Biol."},{"key":"ref52","doi-asserted-by":"publisher","first-page":"1460","DOI":"10.1126\/science.1243444","article-title":"Sources of antimicrobial resistance","volume":"341","author":"Woolhouse","year":"2013","journal-title":"Science"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"20140083","DOI":"10.1098\/rstb.2014.0083","article-title":"Antimicrobial resistance in humans, livestock and the wider environment","volume":"370","author":"Woolhouse","year":"2015","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"560","DOI":"10.1111\/j.1472-765X.2009.02572.x","article-title":"Comparison of antimicrobial resistance patterns between clinical and sewage isolates in a regional hospital in Taiwan","volume":"48","author":"Yang","year":"2009","journal-title":"Lett. Appl. Microbiol."},{"key":"ref55","doi-asserted-by":"publisher","first-page":"2640","DOI":"10.1093\/jac\/dks261","article-title":"Identification of acquired antimicrobial resistance genes","volume":"67","author":"Zankari","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1016\/j.envpol.2012.09.019","article-title":"Comparison of extended-spectrum-beta-lactamase (ESBL) carrying Escherichia coli from sewage sludge and human urinary tract infection","volume":"173","author":"Zarfel","year":"2013","journal-title":"Environ. Pollut."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"968","DOI":"10.1017\/ice.2020.1351","article-title":"Risk factors for carbapenemase-producing organisms among inpatients in Scotland: a national matched case\u2013control study","volume":"42","author":"Zhao","year":"2021","journal-title":"Infect. Control Hosp. Epidemiol."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2021.703560\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,10]],"date-time":"2021-09-10T01:27:22Z","timestamp":1631237242000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2021.703560\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,10]]},"references-count":57,"alternative-id":["10.3389\/fmicb.2021.703560"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2021.703560","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/19006858","asserted-by":"object"}]},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,10]]},"article-number":"703560"}}