{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,1]],"date-time":"2026-02-01T04:30:42Z","timestamp":1769920242647,"version":"3.49.0"},"reference-count":64,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2024,10,16]],"date-time":"2024-10-16T00:00:00Z","timestamp":1729036800000},"content-version":"vor","delay-in-days":289,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"publisher","award":["31003A_182499"],"award-info":[{"award-number":["31003A_182499"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,1,16]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Antibiotic resistance is a growing concern for global health, demanding innovative and effective strategies to combat pathogenic bacteria. Pyoverdines, iron-chelating siderophores produced by environmental Pseudomonas spp., present a novel class of promising compounds to induce growth arrest in pathogens through iron starvation. While we previously demonstrated the efficacy of pyoverdines as antibacterials, our understanding of how these molecules interact with antibiotics and impact resistance evolution remains unknown. Here, we investigated the propensity of three Escherichia coli strains to evolve resistance against pyoverdine, the cephalosporin antibiotic ceftazidime, and their combination. We used a naive E. coli wildtype strain and two isogenic variants carrying the blaTEM-1 \u03b2-lactamase gene on either the chromosome or a costly multicopy plasmid to explore the influence of genetic background on selection for resistance. We found that strong resistance against ceftazidime and weak resistance against pyoverdine evolved in all E. coli variants under single treatment. Ceftazidime resistance was linked to mutations in outer membrane porin genes (envZ and ompF), whereas pyoverdine resistance was associated with mutations in the oligopeptide permease (opp) operon. In contrast, ceftazidime resistance phenotypes were attenuated under combination treatment, especially for the E. coli variant carrying blaTEM-1 on the multicopy plasmid. Altogether, our results show that ceftazidime and pyoverdine interact neutrally and that pyoverdine as an antibacterial is particularly potent against plasmid-carrying E. coli strains, presumably because iron starvation compromises both cellular metabolism and plasmid replication.<\/jats:p>","DOI":"10.1093\/femsml\/uqae021","type":"journal-article","created":{"date-parts":[[2024,10,16]],"date-time":"2024-10-16T00:38:27Z","timestamp":1729039107000},"source":"Crossref","is-referenced-by-count":1,"title":["Pyoverdine\u2013antibiotic combination treatment: its efficacy and effects on resistance evolution in <i>Escherichia coli<\/i>"],"prefix":"10.1093","volume":"5","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2920-3031","authenticated-orcid":false,"given":"Vera","family":"Vollenweider","sequence":"first","affiliation":[{"name":"Department of Quantitative Biomedicine, University of Zurich , Winterthurerstrasse 190, 8057 Zurich ,","place":["Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Flavie","family":"Roncoroni","sequence":"additional","affiliation":[{"name":"Department of Quantitative Biomedicine, University of Zurich , Winterthurerstrasse 190, 8057 Zurich ,","place":["Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4084-6679","authenticated-orcid":false,"given":"Rolf","family":"K\u00fcmmerli","sequence":"additional","affiliation":[{"name":"Department of Quantitative Biomedicine, University of Zurich , Winterthurerstrasse 190, 8057 Zurich ,","place":["Switzerland"]}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2024,10,15]]},"reference":[{"key":"2024122308580172800_bib1","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1016\/j.cell.2007.03.004","article-title":"Molecular mechanisms of antibacterial multidrug resistance","volume":"128","author":"Alekshun","year":"2007","journal-title":"Cell"},{"key":"2024122308580172800_bib2","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S0168-6445(03)00055-X","article-title":"Bacterial iron homeostasis","volume":"27","author":"Andrews","year":"2003","journal-title":"FEMS Microbiol Rev"},{"key":"2024122308580172800_bib3","doi-asserted-by":"crossref","first-page":"3578","DOI":"10.1128\/JB.186.11.3578-3589.2004","article-title":"Recognition of ferric catecholates by FepA","volume":"186","author":"Annamalai","year":"2004","journal-title":"J Bacteriol"},{"key":"2024122308580172800_bib4","doi-asserted-by":"crossref","first-page":"2006.0008","DOI":"10.1038\/msb4100050","article-title":"Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection","volume":"2","author":"Baba","year":"2006","journal-title":"Mol Syst Biol"},{"key":"2024122308580172800_bib5","doi-asserted-by":"crossref","first-page":"20150294","DOI":"10.1098\/rstb.2015.0294","article-title":"Antimicrobial combinations: Bliss independence and Loewe additivity derived from mechanistic multi-hit models","volume":"371","author":"Baeder","year":"2016","journal-title":"Philos Trans R Soc B Biol Sci"},{"key":"2024122308580172800_bib6","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/j.tree.2013.04.002","article-title":"Exploring the costs of horizontal gene transfer","volume":"28","author":"Baltrus","year":"2013","journal-title":"Trends Ecol Evol"},{"key":"2024122308580172800_bib7","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J Comput Biol"},{"key":"2024122308580172800_bib8","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1186\/1471-2164-15-1039","article-title":"Identifying structural variation in haploid microbial genomes from short-read resequencing data using breseq","volume":"15","author":"Barrick","year":"2014","journal-title":"BMC Genomics"},{"key":"2024122308580172800_bib9","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.tim.2017.11.005","article-title":"The search for \u2018evolution-proof\u2019 antibiotics","volume":"26","author":"Bell","year":"2018","journal-title":"Trends Microbiol"},{"key":"2024122308580172800_bib10","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"2024122308580172800_bib11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.mib.2015.05.008","article-title":"Antimicrobial interactions: mechanisms and implications for drug discovery and resistance evolution","volume":"27","author":"Bollenbach","year":"2015","journal-title":"Curr Opin Microbiol"},{"key":"2024122308580172800_bib12","doi-asserted-by":"crossref","first-page":"12350","DOI":"10.1016\/S0021-9258(19)49846-3","article-title":"Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex","volume":"267","author":"Brickman","year":"1992","journal-title":"J Biol Chem"},{"key":"2024122308580172800_bib13","doi-asserted-by":"crossref","first-page":"24155","DOI":"10.1074\/jbc.M110715200","article-title":"EnvZ-OmpR interaction and osmoregulation in Escherichia coli","volume":"277","author":"Cai","year":"2002","journal-title":"J Biol Chem"},{"key":"2024122308580172800_bib14","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s10534-006-9060-9","article-title":"Molecular mechanism of ferricsiderophore passage through the outer membrane receptor proteins of Escherichia coli","volume":"20","author":"Chakraborty","year":"2007","journal-title":"Biometals"},{"key":"2024122308580172800_bib15","article-title":"nplr: n-parameter logistic regression","author":"Commo","year":"2016"},{"key":"2024122308580172800_bib16","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1128\/MMBR.00031-07","article-title":"Structure, function, and evolution of bacterial ATP-binding cassette systems","volume":"72","author":"Davidson","year":"2008","journal-title":"Microbiol Mol Biol Rev"},{"key":"2024122308580172800_bib17","first-page":"165","article-title":"Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq","volume":"1151","author":"Deatherage","year":"2014","journal-title":"Eng Anal Multicell Syst Methods Protoc"},{"key":"2024122308580172800_bib18","doi-asserted-by":"crossref","first-page":"32301","DOI":"10.1074\/jbc.M404343200","article-title":"The binding specificity of OppA determines the selectivity of the oligopeptide ATP-binding cassette transporter","volume":"279","author":"Doeven","year":"2004","journal-title":"J Biol Chem"},{"key":"2024122308580172800_bib19","doi-asserted-by":"crossref","first-page":"2579","DOI":"10.1128\/JB.180.9.2579-2582.1998","article-title":"Coordinated repression in vitro of the divergent fepA-fes promoters of Escherichia coli by the iron uptake regulation (Fur) protein","volume":"180","author":"Escolar","year":"1998","journal-title":"J Bacteriol"},{"key":"2024122308580172800_bib20","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/j.mib.2011.08.003","article-title":"Combination therapies for combating antimicrobial resistance","volume":"14","author":"Fischbach","year":"2011","journal-title":"Curr Opin Microbiol"},{"key":"2024122308580172800_bib21","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1016\/j.tim.2018.12.010","article-title":"Alternatives to conventional antibiotics in the era of antimicrobial resistance","volume":"27","author":"Ghosh","year":"2019","journal-title":"Trends Microbiol"},{"key":"2024122308580172800_bib22","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/nm0307-290","article-title":"Challenges in tuberculosis drug research and development","volume":"13","author":"Ginsberg","year":"2007","journal-title":"Nat Med"},{"key":"2024122308580172800_bib23","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1093\/jac\/dkg406","article-title":"\u03b2-lactam resistance modulated by the overexpression of response regulators of two-component signal transduction systems in Escherichia coli","volume":"52","author":"Hirakawa","year":"2003","journal-title":"J Antimicrob Chemother"},{"key":"2024122308580172800_bib24","doi-asserted-by":"crossref","first-page":"3944","DOI":"10.1128\/jb.176.13.3944-3955.1994","article-title":"Promoter and operator determinants for fur-mediated iron regulation in the bidirectional fepA-fes control region of the Escherichia coli enterobactin gene system","volume":"176","author":"Hunt","year":"1994","journal-title":"J Bacteriol"},{"key":"2024122308580172800_bib25","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.2741\/1233","article-title":"Three paradoxes of ferric enterobactin uptake","volume":"8","author":"Klebba","year":"2003","journal-title":"Front Biosci"},{"key":"2024122308580172800_bib26","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.jmb.2011.09.043","article-title":"Escherichia coli peptide binding protein OppA has a preference for positively charged peptides","volume":"414","author":"Klepsch","year":"2011","journal-title":"J Mol Biol"},{"key":"2024122308580172800_bib27","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1016\/S0140-6736(09)60918-1","article-title":"Safety and efficacy of raltegravir-based versus efavirenz-based combination therapy in treatment-naive patients with HIV-1 infection: a multicentre, double-blind randomised controlled trial","volume":"374","author":"Lennox","year":"2009","journal-title":"Lancet North Am Ed"},{"key":"2024122308580172800_bib28","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and accurate short read alignment with Burrows\u2013Wheeler transform","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2024122308580172800_bib29","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1046\/j.1365-2958.1998.00764.x","article-title":"The Escherichia coli ATP-binding cassette (ABC) proteins","volume":"28","author":"Linton","year":"1998","journal-title":"Mol Microbiol"},{"key":"2024122308580172800_bib30","doi-asserted-by":"crossref","first-page":"5324","DOI":"10.1128\/AAC.00678-15","article-title":"In vitro selection of ceftazidime-avibactam resistance in Enterobacteriaceae with KPC-3 carbapenemase","volume":"59","author":"Livermore","year":"2015","journal-title":"Antimicrob Agents Chemother"},{"key":"2024122308580172800_bib31","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1136\/bmj.331.7519.706","article-title":"Antimalarial treatment with artemisinin combination therapy in Africa","volume":"331","author":"Malenga","year":"2005","journal-title":"BMJ"},{"key":"2024122308580172800_bib32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s42003-022-04035-y","article-title":"Cephalosporin translocation across enterobacterial OmpF and OmpC channels, a filter across the outer membrane","volume":"5","author":"Masi","year":"2022","journal-title":"Commun Biol"},{"key":"2024122308580172800_bib33","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.resmic.2019.10.005","article-title":"Between computational predictions and high-throughput transcriptional profiling: in depth expression analysis of the OppB trans-membrane subunit of Escherichia coli OppABCDF oligopeptide transporter","volume":"171","author":"Masulis","year":"2020","journal-title":"Res Microbiol"},{"key":"2024122308580172800_bib34","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/0307-4412(83)90043-2","article-title":"Bacteria, iron and pathogenicity","volume":"11","author":"Messenger","year":"1983","journal-title":"Biochem Educ"},{"key":"2024122308580172800_bib35","doi-asserted-by":"crossref","first-page":"14918","DOI":"10.1073\/pnas.0800944105","article-title":"Drug interactions modulate the potential for evolution of resistance","volume":"105","author":"Michel","year":"2008","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024122308580172800_bib36","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.3390\/ijms20061255","article-title":"Thinking outside the bug: molecular targets and strategies to overcome antibiotic resistance","volume":"20","author":"Monserrat-Martinez","year":"2019","journal-title":"Int J Mol Sci"},{"key":"2024122308580172800_bib37","doi-asserted-by":"crossref","first-page":"1757","DOI":"10.1016\/j.bbamem.2008.06.009","article-title":"ATP-binding cassette transporters in Escherichia coli","volume":"1778","author":"Moussatova","year":"2008","journal-title":"Biochim Biophys Acta BBA Biomembr"},{"key":"2024122308580172800_bib38","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/S0140-6736(21)02724-0","article-title":"Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis","volume":"399","author":"Murray","year":"2022","journal-title":"Lancet North Am Ed"},{"key":"2024122308580172800_bib39","doi-asserted-by":"crossref","first-page":"2485","DOI":"10.1128\/AAC.44.9.2485-2491.2000","article-title":"Concentration-dependent selection of small phenotypic differences in TEM \u03b2-lactamase-mediated antibiotic resistance","volume":"44","author":"Negri","year":"2000","journal-title":"Antimicrob Agents Chemother"},{"key":"2024122308580172800_bib40","doi-asserted-by":"crossref","first-page":"18857","DOI":"10.1016\/S0021-9258(18)37361-7","article-title":"Transcriptional mapping and nucleotide sequence of the Escherichia coli fepA-fes enterobactin region. Identification of a unique iron-regulated bidirectional promoter","volume":"263","author":"Pettis","year":"1988","journal-title":"J Biol Chem"},{"key":"2024122308580172800_bib41","article-title":"R: a language and environment for statistical computing","author":"R Core Team","year":"2020"},{"key":"2024122308580172800_bib42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/hdy.2010.24","article-title":"What traits are carried on mobile genetic elements, and why?","volume":"106","author":"Rankin","year":"2011","journal-title":"Heredity"},{"key":"2024122308580172800_bib43","doi-asserted-by":"crossref","first-page":"3584","DOI":"10.1073\/pnas.0630018100","article-title":"Enterobactin: an archetype for microbial iron transport","volume":"100","author":"Raymond","year":"2003","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024122308580172800_bib44","doi-asserted-by":"crossref","first-page":"e3000805","DOI":"10.1371\/journal.pbio.3000805","article-title":"Combining antibiotics with antivirulence compounds can have synergistic effects and reverse selection for antibiotic resistance in Pseudomonas aeruginosa","volume":"18","author":"Rezzoagli","year":"2020","journal-title":"PLOS Biol"},{"key":"2024122308580172800_bib45","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1099\/jmm.0.001134","article-title":"Harnessing bacterial interactions to manage infections: a review on the opportunistic pathogen Pseudomonas aeruginosa as a case example","volume":"69","author":"Rezzoagli","year":"2020","journal-title":"J Med Microbiol"},{"key":"2024122308580172800_bib46","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1038\/35073673","article-title":"HIV chemotherapy","volume":"410","author":"Richman","year":"2001","journal-title":"Nature"},{"key":"2024122308580172800_bib47","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1086\/519860","article-title":"Frequency dependence and cooperation: theory and a test with bacteria","volume":"170","author":"Ross-Gillespie","year":"2007","journal-title":"Am Nat"},{"key":"2024122308580172800_bib48","article-title":"RStudio: integrated development environment for R","author":"RStudio Team","year":"2020"},{"key":"2024122308580172800_bib49","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/nrmicro1816","article-title":"Drugs versus bugs: in pursuit of the persistent predator Mycobacterium tuberculosis","volume":"6","author":"Sacchettini","year":"2008","journal-title":"Nat Rev Microbiol"},{"key":"2024122308580172800_bib50","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1111\/j.1574-6976.2010.00222.x","article-title":"Natural evolution of TEM-1 \u03b2-lactamase: experimental reconstruction and clinical relevance","volume":"34","author":"Salverda","year":"2010","journal-title":"FEMS Microbiol Rev"},{"key":"2024122308580172800_bib51","first-page":"1","article-title":"Multicopy plasmids potentiate the evolution of antibiotic resistance in bacteria","volume":"1","author":"San\u00a0Millan","year":"2016","journal-title":"Nat Ecol Evol"},{"key":"2024122308580172800_bib52","doi-asserted-by":"publisher","DOI":"10.1128\/microbiolspec.mtbp-0016-2017","article-title":"Fitness costs of plasmids: a limit to plasmid transmission","volume":"5","author":"San\u00a0Millan","year":"2017","journal-title":"Microbiol Spectr"},{"key":"2024122308580172800_bib53","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1007\/s00726-013-1468-2","article-title":"Fate of ferrisiderophores after import across bacterial outer membranes: different iron release strategies are observed in the cytoplasm or periplasm depending on the siderophore pathways","volume":"44","author":"Schalk","year":"2013","journal-title":"Amino Acids"},{"key":"2024122308580172800_bib54","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"2024122308580172800_bib55","doi-asserted-by":"crossref","first-page":"e79656","DOI":"10.1371\/journal.pone.0079656","article-title":"Analysis and expansion of the role of the Escherichia coli protein ProQ","volume":"8","author":"Sheidy","year":"2013","journal-title":"PLoS One"},{"key":"2024122308580172800_bib56","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1186\/s12859-016-1016-7","article-title":"Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves","volume":"17","author":"Sprouffske","year":"2016","journal-title":"BMC Bioinf"},{"key":"2024122308580172800_bib57","doi-asserted-by":"crossref","first-page":"e02071","DOI":"10.1128\/aac.02071-21","article-title":"Considerations for the use of phage therapy in clinical practice","volume":"66","author":"Suh","year":"2022","journal-title":"Antimicrob Agents Chemother"},{"key":"2024122308580172800_bib58","doi-asserted-by":"crossref","first-page":"e208","DOI":"10.1016\/S1473-3099(21)00612-5","article-title":"Safety and efficacy of phage therapy in difficult-to-treat infections: a systematic review","volume":"22","author":"Uyttebroek","year":"2022","journal-title":"Lancet Infect Dis"},{"key":"2024122308580172800_bib59","first-page":"277","article-title":"The antibiotic resistance crisis","volume":"40","author":"Ventola","year":"2015","journal-title":"Pharm Ther"},{"key":"2024122308580172800_bib60","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1038\/s41579-019-0294-2","article-title":"Porins and small-molecule translocation across the outer membrane of Gram-negative bacteria","volume":"18","author":"Vergalli","year":"2020","journal-title":"Nat Rev Microbiol"},{"key":"2024122308580172800_bib61","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1111\/eva.12202","article-title":"The genetic basis of the fitness costs of antimicrobial resistance: a meta-analysis approach","volume":"8","author":"Vogwill","year":"2015","journal-title":"Evol Appl"},{"key":"2024122308580172800_bib62","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.92493.1","article-title":"Antimicrobial activity of iron-depriving pyoverdines against human opportunistic pathogens","volume":"13","author":"Vollenweider","year":"2024","journal-title":"eLife"},{"key":"2024122308580172800_bib63","doi-asserted-by":"crossref","first-page":"13774","DOI":"10.1073\/pnas.1715874115","article-title":"Resource limitation prevents the emergence of drug resistance by intensifying within-host competition","volume":"114","author":"Wale","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"key":"2024122308580172800_bib64","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1038\/s41598-020-58014-6","article-title":"Conversion of broad-spectrum antimicrobial peptides into species-specific antimicrobials capable of precisely targeting pathogenic bacteria","volume":"10","author":"Xu","year":"2020","journal-title":"Sci Rep"}],"container-title":["microLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/microlife\/advance-article-pdf\/doi\/10.1093\/femsml\/uqae021\/59766158\/uqae021.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/microlife\/article-pdf\/doi\/10.1093\/femsml\/uqae021\/61017362\/uqae021.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/microlife\/article-pdf\/doi\/10.1093\/femsml\/uqae021\/61017362\/uqae021.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,23]],"date-time":"2024-12-23T08:58:34Z","timestamp":1734944314000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/microlife\/article\/doi\/10.1093\/femsml\/uqae021\/7823299"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024]]},"references-count":64,"URL":"https:\/\/doi.org\/10.1093\/femsml\/uqae021","relation":{},"ISSN":["2633-6693"],"issn-type":[{"value":"2633-6693","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024]]},"published":{"date-parts":[[2024]]},"article-number":"uqae021"}}