{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T08:59:11Z","timestamp":1792141151741,"version":"4.4.0"},"update-to":[{"DOI":"10.1371\/journal.ppat.1012491","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,3,10]],"date-time":"2025-03-10T00:00:00Z","timestamp":1741564800000}}],"reference-count":61,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2025,3,3]],"date-time":"2025-03-03T00:00:00Z","timestamp":1740960000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100006492","name":"Division of Intramural Research, National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["AI132356"],"award-info":[{"award-number":["AI132356"]}],"id":[{"id":"10.13039\/100006492","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32GM007270"],"award-info":[{"award-number":["T32GM007270"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p><jats:italic>Listeria monocytogenes<\/jats:italic> is a Gram-positive pathogen that causes the severe foodborne disease listeriosis. Following oral infection of the host, <jats:italic>L. monocytogenes<\/jats:italic> disseminates from the gastrointestinal tract to peripheral organs, including the gallbladder, where it replicates to high densities, establishing the gallbladder as the primary bacterial reservoir. Despite its importance in pathogenesis, little is known about how <jats:italic>L. monocytogenes<\/jats:italic> survives and replicates in the gallbladder. In this study, we assessed the <jats:italic>L. monocytogenes<\/jats:italic> genes required for growth and survival in <jats:italic>ex vivo<\/jats:italic> non-human primate gallbladders using a transposon sequencing approach. The screen identified 43 genes required for replication in the gallbladder, some of which were known to be important for virulence, and others had not been previously studied in the context of infection. We evaluated the roles of 19 genes identified in our screen both <jats:italic>in vitro<\/jats:italic> and <jats:italic>in vivo<\/jats:italic>, and demonstrate that most were required for replication in bile <jats:italic>in vitro<\/jats:italic>, for intracellular infection of murine cells in tissue culture, and for virulence in an oral murine model of listeriosis. Interestingly, strains lacking the mannose and glucose phosphoenolpyruvate-dependent phosphotransferase system (PTS) permeases Mpt and Mpo exhibited no defects in intracellular growth or intercellular spread, but were significantly attenuated during murine infection. While the roles of PTS systems <jats:italic>in vivo<\/jats:italic> were not previously appreciated, these results suggest that PTS permeases are necessary for extracellular replication during infection. Overall, this study demonstrates that <jats:italic>L. monocytogenes<\/jats:italic> genes required for replication in the gallbladder also play broader roles in disease.<\/jats:p>","DOI":"10.1371\/journal.ppat.1012491","type":"journal-article","created":{"date-parts":[[2025,3,3]],"date-time":"2025-03-03T18:27:20Z","timestamp":1741026440000},"page":"e1012491","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["A genome-wide screen in ex vivo gallbladders identifies Listeria monocytogenes factors required for virulence in vivo"],"prefix":"10.1371","volume":"21","author":[{"given":"Nicole H.","family":"Schwardt","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cortney R.","family":"Halsey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Madison E.","family":"Sanchez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Billy M.","family":"Ngo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0770-7784","authenticated-orcid":true,"given":"Michelle L.","family":"Reniere","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,3,3]]},"reference":[{"issue":"1","key":"ppat.1012491.ref001","doi-asserted-by":"crossref","first-page":"6826","DOI":"10.1038\/s41467-021-27069-y","article-title":"Listeria monocytogenes faecal carriage is common and depends on the gut microbiota","volume":"12","author":"L Hafner","year":"2021","journal-title":"Nat Commun"},{"key":"ppat.1012491.ref002","doi-asserted-by":"crossref","unstructured":"EFSA Panel on Biological Hazards (BIOHAZ), Ricci A, Allende A, Bolton D, Chemaly M, Davies R, et al. Listeria monocytogenes contamination of ready\u2010to\u2010eat foods and the risk for human health in the EU. EFS2. 2018;16. 10.2903\/j.efsa.2018.5134","DOI":"10.2903\/j.efsa.2018.5134"},{"issue":"10","key":"ppat.1012491.ref003","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1056\/NEJMoa1215837","article-title":"Multistate outbreak of listeriosis associated with cantaloupe","volume":"369","author":"JT McCollum","year":"2013","journal-title":"N Engl J Med"},{"issue":"6","key":"ppat.1012491.ref004","doi-asserted-by":"crossref","first-page":"e02948-19","DOI":"10.1128\/mBio.02948-19","article-title":"A Multiorgan Trafficking Circuit Provides Purifying Selection of Listeria monocytogenes Virulence Genes","volume":"10","author":"A Louie","year":"2019","journal-title":"mBio"},{"issue":"2","key":"ppat.1012491.ref005","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1128\/IAI.05958-11","article-title":"Oral infection with signature-tagged Listeria monocytogenes reveals organ-specific growth and dissemination routes in guinea pigs","volume":"80","author":"JA Melton-Witt","year":"2012","journal-title":"Infect Immun"},{"issue":"4","key":"ppat.1012491.ref006","doi-asserted-by":"crossref","first-page":"e0006423","DOI":"10.1128\/iai.00064-23","article-title":"Egress of Listeria monocytogenes from Mesenteric Lymph Nodes Depends on Intracellular Replication and Cell-to-Cell Spread","volume":"91","author":"JS Tucker","year":"2023","journal-title":"Infect Immun"},{"issue":"24","key":"ppat.1012491.ref007","doi-asserted-by":"crossref","first-page":"6334","DOI":"10.1073\/pnas.1702077114","article-title":"Deciphering the landscape of host barriers to Listeria monocytogenes infection","volume":"114","author":"T Zhang","year":"2017","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"3","key":"ppat.1012491.ref008","doi-asserted-by":"crossref","first-page":"1819","DOI":"10.1128\/IAI.74.3.1819-1827.2006","article-title":"Induced biliary excretion of Listeria monocytogenes","volume":"74","author":"J Hardy","year":"2006","journal-title":"Infect Immun"},{"issue":"4","key":"ppat.1012491.ref009","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1016\/j.femsre.2004.09.003","article-title":"The interaction between bacteria and bile","volume":"29","author":"M Begley","year":"2005","journal-title":"FEMS Microbiol Rev"},{"issue":"5659","key":"ppat.1012491.ref010","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1126\/science.1092712","article-title":"Extracellular replication of Listeria monocytogenes in the murine gall bladder","volume":"303","author":"J Hardy","year":"2004","journal-title":"Science"},{"issue":"11","key":"ppat.1012491.ref011","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1016\/j.tim.2014.06.007","article-title":"Salmonella chronic carriage: epidemiology, diagnosis, and gallbladder persistence","volume":"22","author":"JS Gunn","year":"2014","journal-title":"Trends in Microbiology"},{"key":"ppat.1012491.ref012","doi-asserted-by":"crossref","first-page":"940","DOI":"10.3389\/fmicb.2017.00940","article-title":"RNAseq Reveals Complex Response of Campylobacter jejuni to Ovine Bile and In vivo Gallbladder Environment","volume":"8","author":"AJ Kreuder","year":"2017","journal-title":"Front Microbiol"},{"issue":"8","key":"ppat.1012491.ref013","doi-asserted-by":"crossref","first-page":"2920","DOI":"10.1128\/IAI.00258-13","article-title":"Gallbladder epithelium as a niche for chronic Salmonella carriage","volume":"81","author":"G Gonzalez-Escobedo","year":"2013","journal-title":"Infect Immun"},{"key":"ppat.1012491.ref014","doi-asserted-by":"crossref","first-page":"226","DOI":"10.3389\/fvets.2019.00226","article-title":"Histopathology and Spatial Distribution of Putative Growth Factors in Relation to Bacterial Localization of Campylobacter jejuni Within the Ovine Gallbladder","volume":"6","author":"AJ Kreuder","year":"2019","journal-title":"Front Vet Sci"},{"issue":"1","key":"ppat.1012491.ref015","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1194\/jlr.M500180-JLR200","article-title":"Gallbladder histopathology during murine gallstone formation: relation to motility and concentrating function","volume":"47","author":"KJ van Erpecum","year":"2006","journal-title":"J Lipid Res"},{"issue":"9","key":"ppat.1012491.ref016","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1038\/s41576-020-0244-x","article-title":"A decade of advances in transposon-insertion sequencing","volume":"21","author":"AK Cain","year":"2020","journal-title":"Nat Rev Genet"},{"issue":"10","key":"ppat.1012491.ref017","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1038\/nmeth.1377","article-title":"Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms","volume":"6","author":"T van Opijnen","year":"2009","journal-title":"Nat Methods"},{"issue":"5","key":"ppat.1012491.ref018","doi-asserted-by":"crossref","first-page":"e01729-14","DOI":"10.1128\/mBio.01729-14","article-title":"Genes contributing to Staphylococcus aureus fitness in abscess- and infection-related ecologies","volume":"5","author":"MD Valentino","year":"2014","journal-title":"mBio"},{"key":"ppat.1012491.ref019","doi-asserted-by":"crossref","unstructured":"Shull LM, Camilli A. Transposon Sequencing of Vibrio cholerae in the Infant Rabbit Model of Cholera. Vibrio Cholerae: Methods and Protocols. New York, NY: Springer; 2018. pp. 103\u2013116. 10.1007\/978-1-4939-8685-9_10","DOI":"10.1007\/978-1-4939-8685-9_10"},{"issue":"8","key":"ppat.1012491.ref020","doi-asserted-by":"crossref","first-page":"e0133224","DOI":"10.1128\/mbio.01332-24","article-title":"RECON gene disruption enhances host resistance to enable genome-wide evaluation of intracellular pathogen fitness during infection","volume":"15","author":"CE Stamm","year":"2024","journal-title":"mBio"},{"issue":"1","key":"ppat.1012491.ref021","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1128\/IAI.00330-10","article-title":"Investigation of the mechanisms by which Listeria monocytogenes grows in porcine gallbladder bile","volume":"79","author":"GC Dowd","year":"2011","journal-title":"Infect Immun"},{"issue":"Pt 4","key":"ppat.1012491.ref022","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1099\/mic.0.034934-0","article-title":"The major PEP-phosphotransferase systems (PTSs) for glucose, mannose and cellobiose of Listeria monocytogenes, and their significance for extra- and intracellular growth","volume":"156","author":"R Stoll","year":"2010","journal-title":"Microbiology (Reading)"},{"issue":"4","key":"ppat.1012491.ref023","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1128\/MMBR.00024-06","article-title":"How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria","volume":"70","author":"J Deutscher","year":"2006","journal-title":"Microbiol Mol Biol Rev"},{"issue":"6","key":"ppat.1012491.ref024","doi-asserted-by":"crossref","first-page":"151591","DOI":"10.1016\/j.ijmm.2023.151591","article-title":"ListiWiki: A database for the foodborne pathogen Listeria monocytogenes","volume":"313","author":"C Elfmann","year":"2023","journal-title":"Int J Med Microbiol"},{"issue":"Pt 4","key":"ppat.1012491.ref025","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1099\/mic.0.075242-0","article-title":"Identification of genes essential for anaerobic growth of Listeria monocytogenes","volume":"160","author":"S M\u00fcller-Herbst","year":"2014","journal-title":"Microbiology (Reading)"},{"issue":"9","key":"ppat.1012491.ref026","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1038\/nrmicro2171","article-title":"Listeria monocytogenes - from saprophyte to intracellular pathogen","volume":"7","author":"NE Freitag","year":"2009","journal-title":"Nat Rev Microbiol"},{"issue":"7","key":"ppat.1012491.ref027","doi-asserted-by":"crossref","first-page":"1973","DOI":"10.1084\/jem.20170495","article-title":"Commensal microbes provide first line defense against Listeria monocytogenes infection","volume":"214","author":"S Becattini","year":"2017","journal-title":"J Exp Med"},{"issue":"11","key":"ppat.1012491.ref028","doi-asserted-by":"crossref","first-page":"e1003015","DOI":"10.1371\/journal.ppat.1003015","article-title":"InlA promotes dissemination of Listeria monocytogenes to the mesenteric lymph nodes during food borne infection of mice","volume":"8","author":"EN Bou Ghanem","year":"2012","journal-title":"PLoS Pathog"},{"issue":"2","key":"ppat.1012491.ref029","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1128\/IAI.73.2.894-904.2005","article-title":"Contribution of three bile-associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes","volume":"73","author":"M Begley","year":"2005","journal-title":"Infect Immun"},{"issue":"4","key":"ppat.1012491.ref030","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1046\/j.1365-2958.2002.03080.x","article-title":"Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis","volume":"45","author":"O Dussurget","year":"2002","journal-title":"Mol Microbiol"},{"issue":"4","key":"ppat.1012491.ref031","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1111\/j.1365-2958.2004.04454.x","article-title":"A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes","volume":"55","author":"RD Sleator","year":"2005","journal-title":"Mol Microbiol"},{"issue":"29","key":"ppat.1012491.ref032","doi-asserted-by":"crossref","first-page":"10191","DOI":"10.1073\/pnas.0804170105","article-title":"Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity","volume":"105","author":"GT Crimmins","year":"2008","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"5986","key":"ppat.1012491.ref033","doi-asserted-by":"crossref","first-page":"1703","DOI":"10.1126\/science.1189801","article-title":"c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response","volume":"328","author":"JJ Woodward","year":"2010","journal-title":"Science"},{"issue":"1","key":"ppat.1012491.ref034","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1111\/j.1365-2958.2011.07683.x","article-title":"The novel Listeria monocytogenes bile sensor BrtA controls expression of the cholic acid efflux pump MdrT","volume":"81","author":"SJ Quillin","year":"2011","journal-title":"Mol Microbiol"},{"issue":"8","key":"ppat.1012491.ref035","doi-asserted-by":"crossref","first-page":"e1009379","DOI":"10.1371\/journal.ppat.1009379","article-title":"The redox-responsive transcriptional regulator Rex represses fermentative metabolism and is required for Listeria monocytogenes pathogenesis","volume":"17","author":"CR Halsey","year":"2021","journal-title":"PLoS Pathog"},{"issue":"1","key":"ppat.1012491.ref036","doi-asserted-by":"crossref","first-page":"7586","DOI":"10.1038\/s41467-022-35277-3","article-title":"Discovery and structure of a widespread bacterial ABC transporter specific for ergothioneine","volume":"13","author":"Y Zhang","year":"2022","journal-title":"Nat Commun"},{"issue":"5","key":"ppat.1012491.ref037","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1089\/fpd.2011.1013","article-title":"Purine biosynthesis mutants (purA and purB) of serotype 4b Listeria monocytogenes are severely attenuated for systemic infection in intragastrically inoculated A\/J Mice","volume":"9","author":"NG Faith","year":"2012","journal-title":"Foodborne Pathog Dis"},{"issue":"12","key":"ppat.1012491.ref038","doi-asserted-by":"crossref","first-page":"3950","DOI":"10.1128\/JB.00016-09","article-title":"Development of a mariner-based transposon and identification of Listeria monocytogenes determinants, including the peptidyl-prolyl isomerase PrsA2, that contribute to its hemolytic phenotype","volume":"191","author":"J Zemansky","year":"2009","journal-title":"J Bacteriol"},{"issue":"7","key":"ppat.1012491.ref039","doi-asserted-by":"crossref","first-page":"e1005741","DOI":"10.1371\/journal.ppat.1005741","article-title":"An In Vivo Selection Identifies Listeria monocytogenes Genes Required to Sense the Intracellular Environment and Activate Virulence Factor Expression","volume":"12","author":"ML Reniere","year":"2016","journal-title":"PLoS Pathog"},{"issue":"9","key":"ppat.1012491.ref040","doi-asserted-by":"crossref","first-page":"3756","DOI":"10.1128\/iai.61.9.3756-3760.1993","article-title":"Intracytoplasmic growth and virulence of Listeria monocytogenes auxotrophic mutants","volume":"61","author":"H Marquis","year":"1993","journal-title":"Infect Immun"},{"issue":"2\u20133","key":"ppat.1012491.ref041","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/S0168-1605(00)00305-6","article-title":"Analysis of the role of the Listeria monocytogenes F0F1 -AtPase operon in the acid tolerance response","volume":"60","author":"PD Cotter","year":"2000","journal-title":"Int J Food Microbiol"},{"issue":"2","key":"ppat.1012491.ref042","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1128\/JB.00972-06","article-title":"Interference of components of the phosphoenolpyruvate phosphotransferase system with the central virulence gene regulator PrfA of Listeria monocytogenes","volume":"189","author":"S Mertins","year":"2007","journal-title":"J Bacteriol"},{"issue":"5","key":"ppat.1012491.ref043","doi-asserted-by":"crossref","first-page":"e0107423","DOI":"10.1128\/mbio.01074-23","article-title":"The major role of Listeria monocytogenes folic acid metabolism during infection is the generation of N-formylmethionine","volume":"14","author":"Y Feng","year":"2023","journal-title":"mBio"},{"issue":"5","key":"ppat.1012491.ref044","doi-asserted-by":"crossref","first-page":"e0138523","DOI":"10.1128\/mbio.01385-23","article-title":"Listeria monocytogenes folate metabolism is required to generate N-formylmethionine during infection","volume":"14","author":"Q Tang","year":"2023","journal-title":"mBio"},{"issue":"4","key":"ppat.1012491.ref045","first-page":"10.1128\/microbiolspec.gpp3-0066","article-title":"Metabolism of the Gram-Positive Bacterial Pathogen Listeria monocytogenes","volume":"7","author":"J-D Sauer","year":"2019","journal-title":"Microbiol Spectr"},{"issue":"1","key":"ppat.1012491.ref046","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1073\/pnas.012363899","article-title":"Hpt, a bacterial homolog of the microsomal glucose- 6-phosphate translocase, mediates rapid intracellular proliferation in Listeria","volume":"99","author":"I Chico-Calero","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"2","key":"ppat.1012491.ref047","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1128\/JB.188.2.556-568.2006","article-title":"Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening","volume":"188","author":"B Joseph","year":"2006","journal-title":"J Bacteriol"},{"issue":"1","key":"ppat.1012491.ref048","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1111\/j.1365-2958.2011.07692.x","article-title":"Mutational analysis of glucose transport regulation and glucose-mediated virulence gene repression in Listeria monocytogenes","volume":"81","author":"FMD Ak\u00e9","year":"2011","journal-title":"Mol Microbiol"},{"issue":"8","key":"ppat.1012491.ref049","doi-asserted-by":"crossref","first-page":"3146","DOI":"10.1128\/IAI.00503-15","article-title":"Intracellular Listeria monocytogenes comprises a minimal but vital fraction of the intestinal burden following foodborne infection","volume":"83","author":"GS Jones","year":"2015","journal-title":"Infect Immun"},{"issue":"6","key":"ppat.1012491.ref050","doi-asserted-by":"crossref","first-page":"2005","DOI":"10.4049\/jimmunol.139.6.2005","article-title":"Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements","volume":"139","author":"DK Bishop","year":"1987","journal-title":"J Immunol"},{"issue":"2","key":"ppat.1012491.ref051","doi-asserted-by":"crossref","first-page":"e00969-14","DOI":"10.1128\/mBio.00969-14","article-title":"Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD-e highlights genomic variations underlying differences in pathogenicity","volume":"5","author":"C B\u00e9cavin","year":"2014","journal-title":"mBio"},{"issue":"9","key":"ppat.1012491.ref052","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1038\/nbt1183-784","article-title":"A Broad Host Range Mobilization System for In Vivo Genetic Engineering: Transposon Mutagenesis in Gram Negative Bacteria","volume":"1","author":"R Simon","year":"1983","journal-title":"Nat Biotechnol"},{"issue":"1","key":"ppat.1012491.ref053","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1111\/j.1365-2958.1993.tb01211.x","article-title":"Dual roles of plcA in Listeria monocytogenes pathogenesis","volume":"8","author":"A Camilli","year":"1993","journal-title":"Mol Microbiol"},{"issue":"6","key":"ppat.1012491.ref054","doi-asserted-by":"crossref","first-page":"e02927-16","DOI":"10.1128\/AEM.02927-16","article-title":"An Effective Counterselection System for Listeria monocytogenes and Its Use To Characterize the Monocin Genomic Region of Strain 10403S","volume":"83","author":"T Argov","year":"2017","journal-title":"Appl Environ Microbiol"},{"issue":"15","key":"ppat.1012491.ref055","doi-asserted-by":"crossref","first-page":"4177","DOI":"10.1128\/JB.184.15.4177-4186.2002","article-title":"Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors","volume":"184","author":"P Lauer","year":"2002","journal-title":"J Bacteriol"},{"issue":"Database issue","key":"ppat.1012491.ref056","first-page":"D581-91","article-title":"PATRIC, the bacterial bioinformatics database and analysis resource","volume":"42","author":"AR Wattam","year":"2014","journal-title":"Nucleic Acids Res"},{"issue":"D1","key":"ppat.1012491.ref057","doi-asserted-by":"crossref","first-page":"D535","DOI":"10.1093\/nar\/gkw1017","article-title":"Improvements to PATRIC, the all-bacterial Bioinformatics Database and Analysis Resource Center","volume":"45","author":"AR Wattam","year":"2017","journal-title":"Nucleic Acids Res"},{"issue":"10","key":"ppat.1012491.ref058","doi-asserted-by":"crossref","first-page":"e1004401","DOI":"10.1371\/journal.pcbi.1004401","article-title":"TRANSIT--A Software Tool for Himar1 TnSeq Analysis","volume":"11","author":"MA DeJesus","year":"2015","journal-title":"PLoS Comput Biol"},{"issue":"4","key":"ppat.1012491.ref059","doi-asserted-by":"crossref","first-page":"1459","DOI":"10.1084\/jem.167.4.1459","article-title":"Role of hemolysin for the intracellular growth of Listeria monocytogenes","volume":"167","author":"DA Portnoy","year":"1988","journal-title":"J Exp Med"},{"issue":"11","key":"ppat.1012491.ref060","doi-asserted-by":"crossref","first-page":"3770","DOI":"10.1128\/iai.58.11.3770-3778.1990","article-title":"Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread","volume":"58","author":"AN Sun","year":"1990","journal-title":"Infect Immun"},{"issue":"7","key":"ppat.1012491.ref061","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH Image to ImageJ: 25 years of image analysis","volume":"9","author":"CA Schneider","year":"2012","journal-title":"Nat Methods"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1012491","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,3,10]],"date-time":"2025-03-10T00:00:00Z","timestamp":1741564800000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1012491","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,10]],"date-time":"2025-03-10T17:44:46Z","timestamp":1741628686000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1012491"}},"subtitle":[],"editor":[{"given":"Mary X.","family":"O'Riordan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,3,3]]},"references-count":61,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,3,3]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1012491","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.ppat.1012491","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,3]]}}}