{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,27]],"date-time":"2026-08-27T07:24:34Z","timestamp":1787815474187,"version":"build-2784847793"},"reference-count":62,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2023,3,8]],"date-time":"2023-03-08T00:00:00Z","timestamp":1678233600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Alliance for Food Safety and Security grant (USDA)","award":["2018-07464"],"award-info":[{"award-number":["2018-07464"]}]},{"DOI":"10.13039\/100000199","name":"USDA National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["2018-07464"],"award-info":[{"award-number":["2018-07464"]}],"id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Listeria monocytogenes is a Gram-positive pathogen responsible for the severe foodborne disease listeriosis. A chromosomal hotspot between lmo0301 and lmo0305 has been noted to harbor diverse restriction modification (RM) systems. Here, we analyzed 872 L. monocytogenes genomes to better understand the prevalence and types of RM systems in this region, designated the immigration control region (ICR). Type I, II, III and IV RM systems were found in 86.1% of strains inside the ICR and in 22.5% of strains flanking the ICR. ICR content was completely conserved within the same multilocus sequence typing-based sequence type (ST), but the same RM system could be identified in diverse STs. The intra-ST conservation of ICR content suggests that this region may drive the emergence of new STs and promote clone stability. Sau3AI-like, LmoJ2 and LmoJ3 type II RM systems as well as type I EcoKI-like, and type IV AspBHI-like and mcrB-like systems accounted for all RM systems in the ICR. A Sau3AI-like type II RM system with specificity for GATC was harbored in the ICR of many STs, including all strains of the ancient, ubiquitous ST1. The extreme paucity of GATC recognition sites in lytic phages may reflect ancient adaptation of these phages to preempt resistance associated with the widely distributed Sau3AI-like systems. These findings indicate that the ICR has a high propensity for RM systems which are intraclonaly conserved and may impact bacteriophage susceptibility as well as ST emergence and stability.<\/jats:p>","DOI":"10.3390\/microorganisms11030699","type":"journal-article","created":{"date-parts":[[2023,3,9]],"date-time":"2023-03-09T02:33:16Z","timestamp":1678329196000},"page":"699","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Investigation of a Listeria monocytogenes Chromosomal Immigration Control Region Reveals Diverse Restriction Modification Systems with Complete Sequence Type Conservation"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9213-6639","authenticated-orcid":false,"given":"Phillip","family":"Brown","sequence":"first","affiliation":[{"name":"Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6318-0203","authenticated-orcid":false,"given":"Sangmi","family":"Lee","sequence":"additional","affiliation":[{"name":"Department of Food and Nutrition, Chungbuk National University, Chengju 28644, Chungbuk, Republic of Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Driss","family":"Elhanafi","sequence":"additional","affiliation":[{"name":"Biomanufacturing Training and Education Center, North Carolina State University, Raleigh, NC 27695, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6903-5322","authenticated-orcid":false,"given":"Wilhelm","family":"Tham","sequence":"additional","affiliation":[{"name":"School of Hospitality, Culinary Arts and Meal Science, \u00d6rebro University, 702 81 \u00d6rebro, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie-Louise","family":"Danielsson-Tham","sequence":"additional","affiliation":[{"name":"School of Hospitality, Culinary Arts and Meal Science, \u00d6rebro University, 702 81 \u00d6rebro, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gloria","family":"Lopez-Valladares","sequence":"additional","affiliation":[{"name":"School of Hospitality, Culinary Arts and Meal Science, \u00d6rebro University, 702 81 \u00d6rebro, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Chen","sequence":"additional","affiliation":[{"name":"Division of Microbiology, Center for Food Safety and Applied Nutrition, Food and Drug Administration, College Park, MD 20740, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mirena","family":"Ivanova","sequence":"additional","affiliation":[{"name":"Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, 2800 Lyngby, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5674-0142","authenticated-orcid":false,"given":"Pimlapas","family":"Leekitcharoenphon","sequence":"additional","affiliation":[{"name":"Research Group for Genomic Epidemiology, National Food Institute, Technical University of Denmark, 2800 Lyngby, Denmark"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophia","family":"Kathariou","sequence":"additional","affiliation":[{"name":"Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695, USA"},{"name":"Department of Food, Bioprocessing and Nutrition Sciences, North Carolina State University, Raleigh, NC 27695, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1016\/S1473-3099(14)70870-9","article-title":"The global burden of listeriosis: A systematic review and meta-analysis","volume":"14","author":"Devleesschauwer","year":"2014","journal-title":"Lancet Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1038\/nrmicro.2017.126","article-title":"Listeria monocytogenes: Towards a complete picture of its physiology and pathogenesis","volume":"16","author":"Radoshevich","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Ryser, E.T., and Marth., E.H. (2007). Listeriosis in Humans. Listeria, Listeriosis, and Food Safety, CRC Press. [3rd ed.].","DOI":"10.1201\/9781420015188"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Gurtler, J., Doyle, M., and Kornacki, J. (2017). Foodborne Pathogens. Food Microbiology and Food Safety, Springer.","DOI":"10.1007\/978-3-319-56836-2"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2488","DOI":"10.1038\/s41467-019-10380-0","article-title":"Hypervirulent Listeria monocytogenes clones\u2019 adaption to mammalian gut accounts for their association with dairy products","volume":"10","author":"Maury","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e00377-19","DOI":"10.1128\/AEM.00377-19","article-title":"Benzalkonium chlorides: Uses, regulatory status, and microbial resistance","volume":"85","author":"Tagkopoulos","year":"2019","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1089\/fpd.2009.0432","article-title":"Reduction of Listeria monocytogenes on the surface of fresh channel catfish fillets by bacteriophage Listex P100","volume":"7","author":"Soni","year":"2010","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.fm.2015.06.006","article-title":"Bacteriophage cocktail significantly reduces or eliminates Listeria monocytogenes contamination on lettuce, apples, cheese, smoked salmon and frozen foods","volume":"52","author":"Perera","year":"2015","journal-title":"Food Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6623","DOI":"10.1128\/AEM.01282-08","article-title":"Host ranges of Listeria-specific bacteriophages from the turkey processing plant environment in the United States","volume":"74","author":"Kim","year":"2008","journal-title":"Appl. Environ. Micrbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1448","DOI":"10.1016\/j.fm.2011.07.001","article-title":"Control of Listeria monocytogenes growth in a ready-to-eat poultry product using a bacteriophage","volume":"28","author":"Bigot","year":"2011","journal-title":"Food Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"94","DOI":"10.4161\/bact.1.2.15662","article-title":"Bacteriophage biocontrol of Listeria monocytogenes on soft ripened white mold and red-smear cheeses","volume":"1","author":"Guenther","year":"2011","journal-title":"Bacteriophage"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.fm.2013.02.012","article-title":"Persistent Listeria monocytogenes subtypes isolated from a smoked fish processing facility included both phage susceptible and resistant isolates","volume":"35","author":"Vongkamjan","year":"2013","journal-title":"Food Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1111\/mmi.13009","article-title":"Bacteriophage predation promotes serovar diversification in Listeria monocytogenes","volume":"97","author":"Eugster","year":"2015","journal-title":"Mol. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Brown, P., Chen, Y., Parsons, C., Brown, E., Loessner, M.J., Shen, Y., and Kathariou, S. (2021). Whole genome sequence analysis of phage-resistant Listeria monocytogenes serotype 1\/2a strains from turkey processing plants. Pathogens, 10.","DOI":"10.3390\/pathogens10020199"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1128\/JB.181.2.418-425.1999","article-title":"Cell wall teichoic acid glycosylation in Listeria monocytogenes serotype 4b requires gtcA, a novel, serogroup-specific gene","volume":"181","author":"Promadej","year":"1999","journal-title":"J. Bacteriol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1128\/AEM.01773-07","article-title":"Teichoic acid glycosylation mediated by gtcA is required for phage adsorption and susceptibility of Listeria monocytogenes serotype 4b","volume":"74","author":"Cheng","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"4229","DOI":"10.1128\/JCM.01032-06","article-title":"Listeria monocytogenes subgroups IIIA, IIIB, and IIIC delineate genetically distinct populations with varied pathogenic potential","volume":"44","author":"Liu","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"7629","DOI":"10.1128\/AEM.01127-08","article-title":"Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates","volume":"74","author":"Ward","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1007\/s12275-011-1006-4","article-title":"Deciphering the biodiversity of Listeria monocytogenes lineage III strains by polyphasic approaches","volume":"49","author":"Zhao","year":"2011","journal-title":"J. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1811","DOI":"10.4315\/0362-028X-65.11.1811","article-title":"Listeria monocytogenes virulence and pathogenicity, a food safety perspective","volume":"65","author":"Kathariou","year":"2002","journal-title":"J. Food Prot."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1236","DOI":"10.1016\/j.micinf.2007.05.011","article-title":"The epidemiology of human listeriosis","volume":"9","author":"Swaminathan","year":"2007","journal-title":"Microbes Infect."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1038\/ng.3501","article-title":"Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity","volume":"48","author":"Maury","year":"2016","journal-title":"Nat. Genet."},{"key":"ref_23","first-page":"229","article-title":"A phage typing system for Listeria monocytogenes and its use in epidemiological studies","volume":"7","author":"Audurier","year":"1984","journal-title":"Clin. Investig. Med."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Sumrall, E.T., Shen, Y., Keller, A.P., Rismondo, J., Pavlou, M., Eugster, M.R., Boulos, S., Disson, O., Thouvenot, P., and Kilcher, S. (2019). Phage resistance at the cost of virulence: Listeria monocytogenes serovar 4b requires galactosylated teichoic acids for InlB-mediated invasion. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1008032"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Hain, T., Ghai, R., Billion, A., Kuenne, C.T., Steinweg, C., Izar, B., Mohamed, W., Mraheil, M.A., Domann, E., and Schaffrath, S. (2012). Comparative genomics and transcriptomics of lineages I, II, and III strains of Listeria monocytogenes. BMC Genomics, 13.","DOI":"10.1186\/1471-2164-13-144"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1016\/j.bbrc.2014.10.018","article-title":"Comparative analysis of CRISPR loci in different Listeria monocytogenes lineages","volume":"454","author":"Di","year":"2014","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Parsons, C., Brown, P., and Kathariou, S. (2021). Use of bacteriophage amended with CRISPR-Cas systems to combat antimicrobial resistance in the bacterial foodborne pathogen Listeria monocytogenes. Antibiotics, 10.","DOI":"10.3390\/antibiotics10030308"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1093\/nar\/gkt990","article-title":"Highlights of the DNA cutters: A short history of the restriction enzymes","volume":"42","author":"Loenen","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1093\/nar\/gkt747","article-title":"The other face of restriction: Modification-dependent enzymes","volume":"42","author":"Loenen","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5577","DOI":"10.1128\/AEM.00648-10","article-title":"Conservation of genomic localization and sequence content of Sau3AI-like restriction-modification gene cassettes among Listeria monocytogenes epidemic clone I and selected strains of serotype 1\/2a","volume":"76","author":"Yildirim","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1995","DOI":"10.1128\/AEM.07086-11","article-title":"A novel restriction-modification system is responsible for temperature-dependent phage resistance in Listeria monocytogenes ECII","volume":"78","author":"Kim","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2623","DOI":"10.1128\/AEM.07203-11","article-title":"Two novel type II restriction-modification systems occupying genomically equivalent locations on the chromosomes of Listeria monocytogenes strains","volume":"78","author":"Lee","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Kuenne, C., Billion, A., Mraheil, M.A., Strittmatter, A., Daniel, R., Goesmann, A., Barbuddhe, S., Hain, T., and Chakraborty, T. (2013). Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics, 14.","DOI":"10.1186\/1471-2164-14-47"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e02091-e16","DOI":"10.1128\/AEM.02091-16","article-title":"Comparative genomics reveals the diversity of restriction-modification systems and DNA methylation sites in Listeria monocytogenes","volume":"83","author":"Chen","year":"2017","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1111\/j.1365-2958.1992.tb01546.x","article-title":"Organization and function of the mcrBC genes of Escherichia coli K-12","volume":"6","author":"Raleigh","year":"1992","journal-title":"Mol. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1016\/j.resmic.2005.07.001","article-title":"Strain variability in the DNA immigration control region (ICR) of Xylella fastidiosa","volume":"157","author":"Picchi","year":"2006","journal-title":"Res. Microbiol."},{"key":"ref_37","unstructured":"Lee, S. (2011). Characterization of the immigration control region of Listeria monocytogenes. [Ph.D. Thesis, North Carolina State University]. Available online: http:\/\/www.lib.ncsu.edu\/resolver\/1840.16\/7955."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"16185","DOI":"10.1038\/nmicrobiol.2016.185","article-title":"Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes","volume":"2","author":"Moura","year":"2016","journal-title":"Nat. Microbiol."},{"key":"ref_39","first-page":"D606","article-title":"The PATRIC Bioinformatics Resource Center: Expanding data and analysis capabilities","volume":"48","author":"Davis","year":"2020","journal-title":"Nucleic Acids Res."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., Formsma, K., Gerdes, S., Glass, E.M., and Kubal, M. (2008). The RAST Server: Rapid annotations using subsystems technology. BMC Genomics, 9.","DOI":"10.1186\/1471-2164-9-75"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1016\/j.jmb.2017.12.007","article-title":"A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core","volume":"430","author":"Zimmermann","year":"2018","journal-title":"J. Mol. Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"D298","DOI":"10.1093\/nar\/gku1046","article-title":"REBASE\u2014A database for DNA restriction and modification: Enzymes, genes and genomes","volume":"43","author":"Roberts","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1093\/bioinformatics\/btm404","article-title":"Clustal W and Clustal X version 2.0","volume":"23","author":"Larkin","year":"2007","journal-title":"Bioinformatics"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3085","DOI":"10.1128\/aem.63.8.3085-3089.1997","article-title":"Host-mediated modification of Sau3AI restriction in Listeria monocytogenes: Prevalence in epidemic-associated strains","volume":"63","author":"Zheng","year":"1997","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e00396-18","DOI":"10.1128\/mBio.00396-18","article-title":"Listeria monocytogenes source distribution analysis indicates regional heterogeneity and ecological niche preference among serotype 4b clones","volume":"9","author":"Lee","year":"2018","journal-title":"mBio"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e0035722","DOI":"10.1128\/aem.00357-22","article-title":"Prevalence and clonal diversity of over 1,200 Listeria monocytogenes isolates collected from public access waters near produce production areas on the central California coast during 2011 to 2016","volume":"88","author":"Gorski","year":"2022","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Iwu, C.D., and Okoh, A.I. (2020). Characterization of antibiogram fingerprints in Listeria monocytogenes recovered from irrigation water and agricultural soil samples. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0228956"},{"key":"ref_49","first-page":"004795","article-title":"Listeria cossartiae sp. nov., Listeria farberi sp. nov., Listeria immobilis sp. nov., Listeria portnoyi sp. nov. and Listeria rustica sp. nov., isolated from agricultural water and natural environments","volume":"71","author":"Carlin","year":"2021","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.ijmm.2010.05.002","article-title":"Listeria monocytogenes lineages: Genomics, evolution, ecology, and phenotypic characteristics","volume":"301","author":"Orsi","year":"2011","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1126\/science.1063447","article-title":"Comparative genomics of Listeria species","volume":"294","author":"Glaser","year":"2001","journal-title":"Science"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"866","DOI":"10.3389\/fmicb.2020.00866","article-title":"Microevolution and gain or loss of mobile genetic elements of outbreak-related Listeria monocytogenes in food processing environments identified by whole genome sequencing analysis","volume":"11","author":"Yang","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1099\/00221287-95-1-166","article-title":"DNA restriction and modification systems in Salmonella. SQ, a new system derived by recombination between the SB system of Salmonella typhimurium and the SP system of Salmonella potsdam","volume":"95","author":"Bullas","year":"1976","journal-title":"J. Gen. Microbiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1093\/nar\/gkt847","article-title":"Type I restriction enzymes and their relatives","volume":"42","author":"Loenen","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1128\/AEM.06378-11","article-title":"Atypical Listeria monocytogenes serotype 4b strains harboring a lineage II-specific gene cassette","volume":"78","author":"Lee","year":"2012","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2309","DOI":"10.1093\/nar\/21.10.2309","article-title":"Gene structure and expression of the MboI restriction\u2013modification system","volume":"21","author":"Ueno","year":"1993","journal-title":"Nucleic Acids Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1093\/nar\/gkt616","article-title":"Type III restriction-modification enzymes: A historical perspective","volume":"42","author":"Rao","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"6039","DOI":"10.1128\/JB.05535-11","article-title":"Defense islands in bacterial and archaeal genomes and prediction of novel defense systems","volume":"193","author":"Makarova","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"4360","DOI":"10.1093\/nar\/gkt157","article-title":"Comparative genomics of defense systems in archaea and bacteria","volume":"41","author":"Makarova","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"5406","DOI":"10.1128\/AAC.00580-10","article-title":"LmrS is a multidrug efflux pump of the major facilitator superfamily from Staphylococcus aureus","volume":"54","author":"Floyd","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1007\/s00253-018-9551-y","article-title":"MdrL, a major facilitator superfamily efflux pump of Listeria monocytogenes involved in tolerance to benzalkonium chloride","volume":"103","author":"Jiang","year":"2019","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"5289","DOI":"10.1021\/acs.chemrev.0c00983","article-title":"Structures and general transport mechanisms by the major facilitator superfamily (MFS)","volume":"121","author":"Drew","year":"2021","journal-title":"Chem. Rev."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/3\/699\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:51:20Z","timestamp":1760122280000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/3\/699"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,8]]},"references-count":62,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,3]]}},"alternative-id":["microorganisms11030699"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11030699","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,8]]}}}