{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,7]],"date-time":"2026-05-07T01:11:44Z","timestamp":1778116304605,"version":"3.51.4"},"reference-count":62,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2020,11,4]],"date-time":"2020-11-04T00:00:00Z","timestamp":1604448000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Salmonella enterica is one of the most common bacterial foodborne pathogens in the United States, causing illnesses that range from self-limiting gastroenteritis to more severe, life threatening invasive disease. Many Salmonella strains contain plasmids that carry virulence, antimicrobial resistance, and\/or transfer genes which allow them to adapt to diverse environments, and these can include incompatibility group (Inc) FIB plasmids. This study was undertaken to evaluate the genomic and phenotypic characteristics of IncFIB-positive Salmonella enterica serovar Typhimurium isolates from food animal sources, to identify their plasmid content, assess antimicrobial resistance and virulence properties, and compare their genotypic isolates with more recently isolated S. Typhimurium isolates from food animal sources. Methods: We identified 71 S. Typhimurium isolates that carried IncFIB plasmids. These isolates were subjected to whole genome sequencing and evaluated for bacteriocin production, antimicrobial susceptibility, the ability to transfer resistance plasmids, and a subset was evaluated for their ability to invade and persist in intestinal human epithelial cells. Results: Approximately 30% of isolates (n = 21) displayed bacteriocin inhibition of Escherichia coli strain J53. Bioinformatic analyses using PlasmidFinder software confirmed that all isolates contained IncFIB plasmids along with multiple other plasmid replicon types. Comparative analyses showed that all strains carried multiple antimicrobial resistance genes and virulence factors including iron acquisition genes, such as iucABCD (75%), iutA (94%), sitABCD (76%) and sitAB (100%). In 17 cases (71%), IncFIB plasmids, along with other plasmid replicon types, were able to conjugally transfer antimicrobial resistance and virulence genes to the susceptible recipient strain. For ten strains, persistence cell counts (27%) were noted to be significantly higher than invasion bacterial cell counts. When the genome sequences of the study isolates collected from 1998\u20132003 were compared to those published from subsequent years (2005\u20132018), overlapping genotypes were found, indicating the perseverance of IncFIB positive strains in food animal populations. This study confirms that IncFIB plasmids can play a potential role in disseminating antimicrobial resistance and virulence genes amongst bacteria from several food animal species.<\/jats:p>","DOI":"10.3390\/genes11111307","type":"journal-article","created":{"date-parts":[[2020,11,5]],"date-time":"2020-11-05T00:00:37Z","timestamp":1604534437000},"page":"1307","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources"],"prefix":"10.3390","volume":"11","author":[{"given":"Nesreen H.","family":"Aljahdali","sequence":"first","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"},{"name":"Biological Science Department, College of Science, King Abdul-Aziz University, Jeddah 21551, Saudi Arabia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bijay K.","family":"Khajanchi","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kennedi","family":"Weston","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"},{"name":"Department of Agriculture, University of Arkansas at Pine Bluff, Pine Bluff, AR 71601, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joanna","family":"Deck","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Justin","family":"Cox","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ruby","family":"Singh","sequence":"additional","affiliation":[{"name":"Office of New Animal Drug Evaluation, U.S. Food and Drug Administration, Center for Veterinary Medicine, Rockville, MD 20855, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeffrey","family":"Gilbert","sequence":"additional","affiliation":[{"name":"Office of New Animal Drug Evaluation, U.S. Food and Drug Administration, Center for Veterinary Medicine, Rockville, MD 20855, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yasser M.","family":"Sanad","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"},{"name":"Department of Agriculture, University of Arkansas at Pine Bluff, Pine Bluff, AR 71601, USA"},{"name":"Department of Parasitology and Animal Diseases, Veterinary Research Division, National Research Centre, Giza 12622, Egypt"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jing","family":"Han","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rajesh","family":"Nayak","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Steven L.","family":"Foley","sequence":"additional","affiliation":[{"name":"Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicological Research, Jefferson, AR 72079, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,11,4]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"7","DOI":"10.3201\/eid1701.P11101","article-title":"Foodborne illness acquired in the united states-major pathogens","volume":"17","author":"Scallan","year":"2011","journal-title":"Emerg. Infect. Dis."},{"key":"ref_2","unstructured":"CDC (2020, March 05). National Enteric Disease Surveillance Salmonella Annual Report, Available online: https:\/\/www.cdc.gov\/salmonella\/index.html."},{"key":"ref_3","unstructured":"USDA (2020, June 15). Cost Estimates of Foodborne Illnesses, Cost of Foodborne Illness Estimates for Salmonella (Non-typhoidal), Available online: https:\/\/www.ers.usda.gov\/data-products\/cost-estimates-of-foodborne-illnesses.aspx#48498."},{"key":"ref_4","unstructured":"Hoffman, S., Maculloch, B., and Batz, M. (2015). Economic burden of major foodborne illnesses acquired in the United States. Econ. Res. Serv."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1128\/MMBR.00015-13","article-title":"Salmonella pathogenicity and host adaptation in chicken-associated serovars","volume":"77","author":"Foley","year":"2013","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_6","unstructured":"CDC (2019, May 23). National Salmonella Surveillance, Available online: https:\/\/www.cdc.gov\/nationalsurveillance\/salmonella-surveillance.html."},{"key":"ref_7","unstructured":"CDC (2019, June 27). An Altas of Salmonella in the United States, 1968\u20132011, Available online: https:\/\/www.cdc.gov\/salmonella\/pdf\/salmonella-atlas-508c.pdf."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1146","DOI":"10.1046\/j.1365-2958.2000.01783.x","article-title":"The putative iron transport system sitabcd encoded on spi1 is required for full virulence of salmonella typhimurium","volume":"35","author":"Janakiraman","year":"2000","journal-title":"Mol. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Winnen, B., Schlumberger, M.C., Sturm, A., Schupbach, K., Siebenmann, S., Jenny, P., and Hardt, W.D. (2008). Hierarchical effector protein transport by the salmonella typhimurium spi-1 type iii secretion system. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0002178"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1574-6968.2010.01904.x","article-title":"So similar, yet so different: Uncovering distinctive features in the genomes of salmonella enterica serovars typhimurium and typhi","volume":"305","author":"Sabbagh","year":"2010","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Han, J., Lynne, A.M., David, D.E., Tang, H.L., Xu, J.S., Nayak, R., Kaldhone, P., Logue, C.M., and Foley, S.L. (2012). DNA sequence analysis of plasmids from multidrug resistant salmonella enterica serotype heidelberg isolates. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0051160"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Khajanchi, B.K., Hasan, N.A., Choi, S.Y., Han, J., Zhao, S.H., Colwell, R.R., Cerniglia, C.E., and Foley, S.L. (2017). Comparative genomic analysis and characterization of incompatibility group fib plasmid encoded virulence factors of salmonella enterica isolated from food sources. BMC Genom., 18.","DOI":"10.1186\/s12864-017-3954-5"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1089\/fpd.2017.2332","article-title":"Evaluation of the genetics and functionality of plasmids in incompatibility group i1-positive salmonella enterica","volume":"15","author":"Kaldhone","year":"2018","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"298","DOI":"10.3389\/fvets.2019.00298","article-title":"Evaluation of incompatibility group i1 (inci1) plasmid-containing salmonella enterica and assessment of the plasmids in bacteriocin production and biofilm development","volume":"6","author":"Kaldhone","year":"2019","journal-title":"Front. Vet. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1111\/jam.12536","article-title":"Demonstration of persistent contamination of a cooked egg product production facility with salmonella enterica serovar Tennessee and characterization of the persistent strain","volume":"117","author":"Jakociune","year":"2014","journal-title":"J. Appl. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"13","DOI":"10.3389\/fmicb.2013.00258","article-title":"Multidrug resistant cornmensal escherichia coli in animals and its impact for public health","volume":"4","author":"Szmolka","year":"2013","journal-title":"Front. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1089\/fpd.2015.2002","article-title":"Molecular characterization of salmonella enterica serovars isolated from a turkey production facility in the absence of selective antimicrobial pressure","volume":"13","author":"Sanad","year":"2016","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e00831-19","DOI":"10.1128\/MRA.00831-19","article-title":"Whole-genome sequences of 35 incompatibility group i1 plasmid-carrying salmonella enterica isolates from food animal and clinical sources","volume":"8","author":"Aljahdali","year":"2019","journal-title":"Microbiol. Resour. Announc."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Aljahdali, N.H., Foley, S.L., Han, J., Sanad, Y.M., Nayak, R., and Khajanchi, B.K. (2020). Whole-genome sequences of 66 incompatibility group fib plasmid-carrying salmonella enterica serovar typhimurium isolates from food animal sources. Microbiol. Resour. Announc., 9.","DOI":"10.1128\/MRA.01435-19"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Khajanchi, B.K., Xu, J., Grim, C.J., Ottesen, A.R., Ramachandran, P., and Foley, S.L. (2019). Global transcriptomic analyses of salmonella enterica in iron-depleted and iron-rich growth conditions. BMC Genom., 20.","DOI":"10.1186\/s12864-019-5768-0"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.vetmic.2015.03.024","article-title":"Interplay between iron homeostasis and virulence: Fur and ryhb as major regulators of bacterial pathogenicity","volume":"179","author":"Porcheron","year":"2015","journal-title":"Vet. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Johnson, T.J., Thorsness, J.L., Anderson, C.P., Lynne, A.M., Foley, S.L., Han, J., Fricke, W.F., McDermott, P.F., White, D.G., and Khatri, M. (2010). Horizontal gene transfer of a colv plasmid has resulted in a dominant avian clonal type of salmonella enterica serovar kentucky. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0015524"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1093\/jac\/dkq181","article-title":"Molecular characterization of addiction systems of plasmids encoding extended-spectrum \u03b2-lactamases in escherichia coli","volume":"65","author":"Mnif","year":"2010","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Mnif, B., Harhour, H., Jdidi, J., Mahjoubi, F., Genel, N., Arlet, G., and Hammami, A. (2013). Molecular epidemiology of extended-spectrum \u03b2-lactamase-producing escherichia coli in tunisia and characterization of their virulence factors and plasmid addiction systems. BMC Microbiol., 13.","DOI":"10.1186\/1471-2180-13-147"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5975","DOI":"10.1128\/JB.00204-06","article-title":"Complete DNA sequence of a colbm plasmid from avian pathogenic escherichia coli suggests that it evolved from closely related colv virulence plasmids","volume":"188","author":"Johnson","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1128\/jcm.34.4.908-911.1996","article-title":"Detection of extended-spectrum \u03b2-lactamases in clinical isolates of klebsiella pneumoniae and escherichia coli","volume":"34","author":"Jacoby","year":"1996","journal-title":"J. Clin. Microbial."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3569","DOI":"10.1128\/JCM.00745-06","article-title":"Comparison of subtyping methods for differentiating salmonella enterica serovar typhimurium isolates obtained from food animal sources","volume":"44","author":"Foley","year":"2006","journal-title":"J. Clin. Microbial."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"5038","DOI":"10.1128\/AEM.00409-08","article-title":"Characterization of salmonella enterica serovar heidelberg from turkey-associated sources","volume":"74","author":"Kaldhone","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.ijantimicag.2009.02.018","article-title":"Characterisation of antibiotic resistance in host-adapted salmonella enterica","volume":"34","author":"Lynne","year":"2009","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1128\/AAC.00842-07","article-title":"Antimicrobial resistance genes associated with salmonella enterica serovar newport isolates from food animals","volume":"52","author":"Lynne","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Gokulan, K., Khare, S., Rooney, A.W., Han, J., Lynne, A.M., and Foley, S.L. (2013). Impact of plasmids, including those encodingvirb4\/d4 type iv secretion systems, on salmonella enterica serovar heidelberg virulence in macrophages and epithelial cells. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0077866"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Welch, T.J., Fricke, W.F., McDermott, P.F., White, D.G., Rosso, M.L., Rasko, D.A., Mammel, M.K., Eppinger, M., Rosovitz, M.J., and Wagner, D. (2007). Multiple antimicrobial resistance in plague: An emerging public health risk. PLoS ONE, 2.","DOI":"10.1371\/journal.pone.0000309"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e20","DOI":"10.7717\/peerj-cs.20","article-title":"Cfsan snp pipeline: An automated method for constructing snp matrices from next-generation sequence data","volume":"1","author":"Davis","year":"2015","journal-title":"PeerJ Comput. Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"W537","DOI":"10.1093\/nar\/gky379","article-title":"The galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update","volume":"46","author":"Afgan","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"Raxml version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies","volume":"30","author":"Stamatakis","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3895","DOI":"10.1128\/AAC.02412-14","article-title":"In silico detection and typing of plasmids using plasmidfinder and plasmid multilocus sequence typing","volume":"58","author":"Carattoli","year":"2014","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_37","doi-asserted-by":"crossref","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":"ref_38","doi-asserted-by":"crossref","first-page":"D581","DOI":"10.1093\/nar\/gkt1099","article-title":"Patric, the bacterial bioinformatics database and analysis resource","volume":"42","author":"Wattam","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"E173","DOI":"10.2527\/jas.2007-0447","article-title":"Food animal-associated salmonella challenges: Pathogenicity and antimicrobial resistance","volume":"86","author":"Foley","year":"2008","journal-title":"J. Anim. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1111\/j.1574-6941.2006.00212.x","article-title":"Horizontal transfer of tet(m) and erm(b) resistance plasmids from food strains of lactobacillus plantarum to enterococcus faecalis jh2-2 in the gastrointestinal tract of gnotobiotic rats","volume":"59","author":"Jacobsen","year":"2007","journal-title":"FEMS Microbiol. Ecol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Nedialkova, L.P., Denzler, R., Koeppel, M.B., Diehl, M., Ring, D., Wille, T., Gerlach, R.G., and Stecher, B. (2014). Inflammation fuels colicin ib-dependent competition of salmonella serovar typhimurium and e. Coli in enterobacterial blooms. PLoS Pathog., 10.","DOI":"10.1371\/journal.ppat.1003844"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1073\/pnas.1113246109","article-title":"Gut inflammation can boost horizontal gene transfer between pathogenic and commensal enterobacteriaceae","volume":"109","author":"Stecher","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3750","DOI":"10.1016\/S0021-9258(19)45098-9","article-title":"Characterization of colicin ia and colicin ib\u2014Chemical studies of protein structure","volume":"247","author":"Konisky","year":"1972","journal-title":"J. Biol. Chem."},{"key":"ref_44","first-page":"533","article-title":"Transcriptional profiling of helicobacter pylori fur- and iron-regulated gene expression","volume":"151","author":"Ernst","year":"2005","journal-title":"Microbiolog"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4538","DOI":"10.1128\/jb.179.14.4538-4544.1997","article-title":"Iron-regulated excretion of \u03b1-keto acids by salmonella typhimurium","volume":"179","author":"Reissbrodt","year":"1997","journal-title":"J. Bacteriol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/S0378-1119(96)00560-4","article-title":"Identification of a new iron regulated locus of salmonella typhi","volume":"183","author":"Baumler","year":"1996","journal-title":"Gene"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Marchetti, M., Bei, O.D., Bettati, S., Campanini, B., Kovachka, S., Gianquinto, E., Spyrakis, F., and Ronda, L. (2020). Iron Metabolism at the Interface between Host and Pathogen: From Nutritional Immunity to Antibacterial Development. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21062145"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1016\/S1286-4579(01)01488-5","article-title":"The salmonella pathogenicity island-1 type iii secretion system","volume":"3","author":"Lostroh","year":"2001","journal-title":"Microb. Infect."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Knodler, L.A., Nair, V., and Steele-Mortimer, O. (2014). Quantitative assessment of cytosolic salmonella in epithelial cells. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0084681"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.ijmm.2017.09.011","article-title":"Seeing is understanding: Salmonella\u2019s way to penetrate the intestinal epithelium","volume":"308","author":"Zhang","year":"2018","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"17733","DOI":"10.1073\/pnas.1006098107","article-title":"Dissemination of invasive salmonella via bacterial-induced extrusion of mucosal epithelia","volume":"107","author":"Knodler","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"3517","DOI":"10.1128\/IAI.00734-16","article-title":"Genetic determinants of salmonella enterica serovar typhimurium proliferation in the cytosol of epithelial cells","volume":"84","author":"Wrande","year":"2016","journal-title":"Infect. Immun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1046\/j.1462-5822.2001.00137.x","article-title":"Intracellular replication of salmonella typhimurium strains in specific subsets of splenic macrophages in vivo","volume":"3","author":"Salcedo","year":"2001","journal-title":"Cell Microbiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2705","DOI":"10.1099\/00221287-148-9-2705","article-title":"Growth and killing of a salmonella enterica serovar typhimurium sifa mutant strain in the cytosol of different host cell lines","volume":"148","author":"Beuzon","year":"2002","journal-title":"Microbiology"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/j.vetmic.2009.02.004","article-title":"In vivo transfer of an incfib plasmid harbouring a class 1 integron with gene cassettes dfra1-aada1","volume":"137","author":"Smith","year":"2009","journal-title":"Vet. Microbiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1128\/mBio.00777-17","article-title":"An in vitro chicken gut model demonstrates transfer of a multidrug resistance plasmid from salmonella to commensal escherichia coli","volume":"8","author":"Card","year":"2017","journal-title":"mBio"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"5523","DOI":"10.1128\/AEM.00020-09","article-title":"Impact of therapeutic treatment with \u03b2-lactam on transfer of the bla(ctx-m-9) resistance gene from salmonella enterica serovar virchow to escherichia coli in gnotobiotic rats","volume":"75","author":"Faure","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1517\/17460441.2012.712512","article-title":"Non-genetic mechanisms communicating antibiotic resistance: Rethinking strategies for antimicrobial drug design","volume":"7","author":"Valvano","year":"2012","journal-title":"Expert Opin. Drug Discov."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.resmic.2010.11.005","article-title":"Environmental factors affecting indole production in escherichia coli","volume":"162","author":"Han","year":"2011","journal-title":"Res. Microbiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1111\/j.1365-2958.2004.04449.x","article-title":"Indole induces the expression of multidrug exporter genes in escherichia coli","volume":"55","author":"Hirakawa","year":"2005","journal-title":"Mol. Microbiol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1038\/nature09354","article-title":"Bacterial charity work leads to population-wide resistance","volume":"467","author":"Lee","year":"2010","journal-title":"Nature"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1006\/scdb.2000.0247","article-title":"Preventing drug access to targets: Cell surface permeability barriers and active efflux in bacteria","volume":"12","author":"Nikaido","year":"2001","journal-title":"Semin. Cell Dev. Biol."}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/11\/1307\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:29:07Z","timestamp":1760178547000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/11\/1307"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,11,4]]},"references-count":62,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11]]}},"alternative-id":["genes11111307"],"URL":"https:\/\/doi.org\/10.3390\/genes11111307","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,4]]}}}