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Volume 9, Issue 11

Plasmid-encoded lactose metabolism and mobilized colistin resistance () genes in serovars isolated from dairy facilities in the 1980s Open Access

Abstract

Horizontal gene transfer by plasmids can confer metabolic capabilities that expand a host cell’s niche. Yet, it is less understood whether the coalescence of specialized catabolic functions, antibiotic resistances and metal resistances on plasmids provides synergistic benefits. In this study, we report whole-genome assembly and phenotypic analysis of five strains isolated in the 1980s from milk powder in Munich, Germany. All strains exhibited the unusual phenotype of lactose-fermentation and encoded either of two variants of the operon. Surprisingly, all strains encoded the mobilized colistin resistance gene 9 (), long before the first report of this gene in the literature. In two cases, the gene and the locus were linked within a large gene island that formed an IncHI2A-type plasmid in one strain but was chromosomally integrated in the other strain. In two other strains, the gene was found on a large IncHI1B/IncP-type plasmid, whereas the locus was encoded on a separate chromosomally integrated plasmidic island. The sequences were identical and genomic contexts could not explain the wide range of colistin resistances exhibited by the strains. Nucleotide variants did explain phenotypic differences in motility and exopolysaccharide production. The observed linkage of to lactose metabolism, an array of heavy-metal detoxification systems, and other antibiotic resistance genes may reflect a coalescence of specialized phenotypes that improve the spread of colistin resistance in dairy facilities, much earlier than previously suspected.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): colistin resistance , comparative genomics , lac genes , lactose , mcr-9 and Salmonella enterica
Funding
This study was supported by the:
  • Natural Sciences and Engineering Research Council of Canada (Award PGS-D)
    • Principle Award Recipient: NicoleA. Lerminiaux
  • Saskatchewan Health Research Foundation (Award #2867)
    • Principle Award Recipient: AndrewD.S. Cameron
  • Natural Sciences and Engineering Research Council of Canada (Award RGPIN-2019-07135)
    • Principle Award Recipient: AndrewD.S. Cameron
  • Natural Sciences and Engineering Research Council of Canada (Award RGPIN-435784-2013)
    • Principle Award Recipient: AndrewD.S. Cameron
  • H2020 Marie Skłodowska-Curie Actions (Award 869441)
    • Principle Award Recipient: AnnaS. Ershova
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2023-11-30
2024-12-03
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References

  1. Dorman MJ, Kane L, Domman D, Turnbull JD, Cormie C et al. The history, genome and biology of NCTC 30: a non-pandemic Vibrio cholerae isolate from World War One. Proc R Soc B Biol Sci 2019; 286:20182025 [View Article] [PubMed]
     [Google Scholar]
  2. Spyrou MA, Musralina L, Gnecchi Ruscone GA, Kocher A, Borbone P-G et al. The source of the black death in fourteenth-century central Eurasia. Nature 2022; 606:718–724 [View Article] [PubMed]
     [Google Scholar]
  3. Twort FW, Hill LE. The fermentation of glucosides by bacteria of the typhoid-coli group and the acquisition of new fermenting powers by bacillus dysenteriæ and other micro-organisms. preliminary communication. Proc R Soc Lond B 1907; 79:329–336 [View Article]
     [Google Scholar]
  4. Leonard SR, Lacher DW, Lampel KA. Acquisition of the lac operon by Salmonella enterica. BMC Microbiol 2015; 15:173 [View Article] [PubMed]
     [Google Scholar]
  5. Lamas A, Miranda JM, Regal P, Vázquez B, Franco CM et al. A comprehensive review of non-enterica subspecies of Salmonella enterica. Microbiol Res 2018; 206:60–73 [View Article] [PubMed]
     [Google Scholar]
  6. McDonough PL, Shin SJ, Lein DH. Diagnostic and public health dilemma of lactose-fermenting Salmonella enterica serotype typhimurium in cattle in the Northeastern United States. J Clin Microbiol 2000; 38:1221–1226 [View Article] [PubMed]
     [Google Scholar]
  7. Mastrorilli E, Pietrucci D, Barco L, Ammendola S, Petrin S et al. n.d. A comparative genomic analysis provides novel insights into the ecological success of the monophasic Salmonella serovar 4,[5],12. Front Microbiol 9: [View Article] [PubMed]
     [Google Scholar]
  8. ISO n.d. International Organization for standardization. General guidance for detection of salmonella. draft method. Technical committee 34, subcommittee 9
     [Google Scholar]
  9. ISO n.d. International Organization for standardization. milk and milk products - detection of salmonella. draft method. Technical committee 34, subcommittee 5
     [Google Scholar]
  10. Kröger C, Fuchs TM. Characterization of the myo-inositol utilization island of Salmonella enterica serovar Typhimurium. J Bacteriol 2009; 191:545–554 [View Article] [PubMed]
     [Google Scholar]
  11. Lehner A, Grimm M, Rattei T, Ruepp A, Frishman D et al. Cloning and characterization of Enterobacter sakazakii pigment genes and in situ spectroscopic analysis of the pigment. FEMS Microbiol Lett 2006; 265:244–248 [View Article] [PubMed]
     [Google Scholar]
  12. Hoiseth SK, Stocker BAD. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981; 291:238–239 [View Article] [PubMed]
     [Google Scholar]
  13. Richardson EJ, Limaye B, Inamdar H, Datta A, Manjari KS et al. Genome sequences of Salmonella enterica serovar Typhimurium, Choleraesuis, Dublin, and Gallinarum strains of well- defined virulence in food-producing animals. J Bacteriol 2011; 193:3162–3163 [View Article] [PubMed]
     [Google Scholar]
  14. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
     [Google Scholar]
  15. Wick RR, Judd LM, Cerdeira LT, Hawkey J, Méric G et al. Trycycler: consensus long-read assemblies for bacterial genomes. Genome Biol 2021; 22:266 [View Article] [PubMed]
     [Google Scholar]
  16. Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 2019; 37:540–546 [View Article]
     [Google Scholar]
  17. Vaser R, Šikić M. Time- and memory-efficient genome assembly with Raven. Nat Comput Sci 2021; 1:332–336 [View Article]
     [Google Scholar]
  18. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation. Genome Res 2017; 27:722–736 [View Article] [PubMed]
     [Google Scholar]
  19. Li H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences. Bioinformatics 2016; 32:2103–2110 [View Article] [PubMed]
     [Google Scholar]
  20. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
     [Google Scholar]
  21. Solares EA, Chakraborty M, Miller DE, Kalsow S, Hall K et al. Rapid low-cost assembly of the Drosophila melanogaster reference genome using low-coverage, long-read sequencing. G3 2018; 8:3143–3154 [View Article] [PubMed]
     [Google Scholar]
  22. Chakraborty M, Baldwin-Brown JG, Long AD, Emerson JJ. Contiguous and accurate de novo assembly of metazoan genomes with modest long read coverage. Nucleic Acids Res 2016; 44:e147 [View Article] [PubMed]
     [Google Scholar]
  23. Wick RR, Judd LM, Gorrie CL, Holt KE, Phillippy AM. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
     [Google Scholar]
  24. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  25. Milne I, Stephen G, Bayer M, Cock PJA, Pritchard L et al. Using tablet for visual exploration of second-generation sequencing data. Brief Bioinform 2013; 14:193–202 [View Article] [PubMed]
     [Google Scholar]
  26. Li H, Birol I. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
     [Google Scholar]
  27. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
     [Google Scholar]
  28. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  29. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
     [Google Scholar]
  30. Robertson J, Nash JHE. MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genom 2018; 4:e000206 [View Article] [PubMed]
     [Google Scholar]
  31. Darling AE, Mau B, Perna NT, Stajich JE. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147 [View Article] [PubMed]
     [Google Scholar]
  32. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high‐quality protein multiple sequence alignments using clustal omega. Mol Syst Biol 2011; 7:539 [View Article] [PubMed]
     [Google Scholar]
  33. Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009; 25:1189–1191 [View Article] [PubMed]
     [Google Scholar]
  34. Seemann T. Snippy: rapid haploid variant calling and core genome alignment. GitHub. n.d https://github. com/tseemann/snippy accessed 19 November 2022
  35. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article] [PubMed]
     [Google Scholar]
  36. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
     [Google Scholar]
  37. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Meth 2012; 9:357–359 [View Article] [PubMed]
     [Google Scholar]
  38. Kröger C, Dillon SC, Cameron ADS, Papenfort K, Sivasankaran SK et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar typhimurium. Proc Natl Acad Sci USA 2012; 109:E1277–E1286 [View Article] [PubMed]
     [Google Scholar]
  39. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  40. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012; 28:3150–3152 [View Article] [PubMed]
     [Google Scholar]
  41. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
     [Google Scholar]
  42. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article] [PubMed]
     [Google Scholar]
  43. European Committee on Antimicrobial Susceptibility Testing (EUCAST) Antimicrobial susceptibility testing EUCAST disk diffusion method. n.d http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Disk_test_documents/ Manual_v_21_EUCAST_Disk_Test.pdf
  44. Carroll LM, Gaballa A, Guldimann C, Sullivan G, Henderson LO et al. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype typhimurium isolate. mBio 2019; e00853-19: [View Article] [PubMed]
     [Google Scholar]
  45. Lee H, Hsu F-F, Turk J, Groisman EA. The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J Bacteriol 2004; 186:4124–4133 [View Article] [PubMed]
     [Google Scholar]
  46. Kröger C, Srikumar S, Ellwart J, Fuchs TM. Bistability in myo-inositol utilization by Salmonella enterica serovar typhimurium. J Bacteriol 2011; 193:1427–1435 [View Article] [PubMed]
     [Google Scholar]
  47. Hellinckx J, Fuchs TM. Hysteresis in myo-inositol utilization by Salmonella typhimurium. MicrobiologyOpen 2017; 6:e00431 [View Article] [PubMed]
     [Google Scholar]
  48. Binet R, Pettengill EA, Hoffmann M, Hammack TS, Monday SR. Construction of stable fluorescent laboratory control strains for several food safety relevant Enterobacteriaceae. Food Microbiology 2018; 76:553–563 [View Article] [PubMed]
     [Google Scholar]
  49. Hindler JA, Humphries RM. Colistin MIC variability by method for contemporary clinical isolates of multidrug-resistant gram-negative bacilli. J Clin Microbiol 2013; 51:1678–1684 [View Article] [PubMed]
     [Google Scholar]
  50. Tyson GH, Li C, Hsu C-H, Ayers S, Borenstein S et al. The Mcr-9 gene of salmonella and Escherichia coli is not associated with colistin resistance in the United States. Antimicrob Agents Chemother 2020e00573-20 [View Article]
     [Google Scholar]
  51. Band VI, Weiss DS, Coers J. Heteroresistance: a cause of unexplained antibiotic treatment failure?. PLOS Pathog 2019; 15:e1007726 [View Article] [PubMed]
     [Google Scholar]
  52. Nicoloff H, Hjort K, Levin BR, Andersson DI. The high prevalence of antibiotic heteroresistance in pathogenic bacteria is mainly caused by gene amplification. Nat Microbiol 2019; 4:504–514 [View Article] [PubMed]
     [Google Scholar]
  53. Tamayo R, Choudhury B, Septer A, Merighi M, Carlson R et al. Identification of cptA, a PmrA-regulated locus required for phosphoethanolamine modification of the Salmonella enterica serovar typhimurium lipopolysaccharide core. J Bacteriol 2005; 187:3391–3399 [View Article] [PubMed]
     [Google Scholar]
  54. Alcock BP, Raphenya AR, Lau TTY, Tsang KK, Bouchard M et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2020; 48:D517–D525 [View Article] [PubMed]
     [Google Scholar]
  55. Alcock BP, Huynh W, Chalil R, Smith KW, Raphenya AR et al. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database. Nucleic Acids Res 2023; 51:D690–D699 [View Article] [PubMed]
     [Google Scholar]
  56. Kadam SK, Rehemtulla A, Sanderson KE. Cloning of rfaG, B, I, and J genes for glycosyltransferase enzymes for synthesis of the lipopolysaccharide core of Salmonella typhimurium. J Bacteriol 1985; 161:277–284 [View Article]
     [Google Scholar]
  57. Kaniuk NA, Vinogradov E, Li J, Monteiro MA, Whitfield C. Chromosomal and plasmid-encoded enzymes are required for assembly of the R3-type core oligosaccharide in the lipopolysaccharide of Escherichia coli O157:H7*. J Biol Chem 2004; 279:31237–31250 [View Article] [PubMed]
     [Google Scholar]
  58. Leipold MD, Kaniuk NA, Whitfield C. The C-terminal domain of the Escherichia coli WaaJ glycosyltransferase is important for catalytic activity and membrane association*. J Biol Chem 2007; 282:1257–1264 [View Article] [PubMed]
     [Google Scholar]
  59. Arai N, Sekizuka T, Tamamura Y, Kusumoto M, Hinenoya A et al. Salmonella genomic island 3 is an integrative and conjugative element and contributes to copper and arsenic tolerance of Salmonella enterica. Antimicrob Agents Chemother 2019; 63:e00429-19 [View Article] [PubMed]
     [Google Scholar]
  60. Branchu P, Charity OJ, Bawn M, Thilliez G, Dallman TJ et al. SGI-4 in monophasic Salmonella Typhimurium ST34 is a novel ICE that enhances resistance to copper. Front Microbiol 2019; 10:1118 [View Article] [PubMed]
     [Google Scholar]
  61. Petrovska L, Mather AE, AbuOun M, Branchu P, Harris SR et al. Microevolution of monophasic Salmonella typhimurium during epidemic, United kingdom, 2005–2010. Emerg Infect Dis 2016; 22:617–624
     [Google Scholar]
  62. Singer HM, Erhardt M, Hughes KT. Comparative analysis of the secretion capability of early and late flagellar type III secretion substrates. Mol Microbiol 2014; 93:505–520 [View Article] [PubMed]
     [Google Scholar]
  63. Homma M, Kutsukake K, Hasebe M, Iino T, Macnab RM. Flgf and Flgg: a family of structurally related proteins in the flagellar basal body of Salmonella typhimurium. J Mol Biol 1990; 211:465–477 [View Article] [PubMed]
     [Google Scholar]
  64. Juhas M, Ajioka JW, Isalan M. Identification and validation of novel chromosomal integration and expression Loci in Escherichia coli flagellar region 1. PLoS One 2015; 10:e0123007 [View Article] [PubMed]
     [Google Scholar]
  65. Blackburn BO, Ellis EM. Lactose-fermenting Salmonella from dried milk and milk-drying plants. Appl Microbiol 1973; 26:672–674 [View Article] [PubMed]
     [Google Scholar]
  66. Jiang L, Ni Z, Wang L, Feng L, Liu B. Loss of the lac operon contributes to Salmonella invasion of epithelial cells through derepression of flagellar synthesis. Curr Microbiol 2015; 70:315–323 [View Article] [PubMed]
     [Google Scholar]
  67. Catry B, Cavaleri M, Baptiste K, Grave K, Grein K et al. Use of colistin-containing products within the European Union and European Economic Area (EU/EEA): development of resistance in animals and possible impact on human and animal health. Int J Antimicrob Agents 2015; 46:297–306 [View Article] [PubMed]
     [Google Scholar]
  68. Binsker U, Käsbohrer A, Hammerl JA. Global colistin use: a review of the emergence of resistant Enterobacterales and the impact on their genetic basis. FEMS Microbiol Rev 2022; 46:fuab049 [View Article] [PubMed]
     [Google Scholar]
  69. Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 2016; 16:161–168 [View Article] [PubMed]
     [Google Scholar]
  70. Shen Z, Wang Y, Shen Y, Shen J, Wu C. Early emergence of mcr-1 in Escherichia coli from food-producing animals. Lancet Infect Dis 2016; 16:293 [View Article] [PubMed]
     [Google Scholar]
  71. Portes AB, Rodrigues G, Leitão MP, Ferrari R, Conte Junior CA. Global distribution of plasmid-mediated colistin resistance mcr gene in Salmonella: a systematic review. J Appl Microbiol 2022; 132:872–889 [View Article] [PubMed]
     [Google Scholar]
  72. Hussein NH, AL-Kadmy IMS, Taha BM, Hussein JD. Mobilized colistin resistance (mcr) genes from 1 to 10: a comprehensive review. Mol Biol Rep 2021; 48:2897–2907 [View Article] [PubMed]
     [Google Scholar]
  73. Luo Q, Wu Y, Bao D, Xu L, Chen H et al. Genomic epidemiology of mcr carrying multidrug-resistant ST34 Salmonella enterica serovar Typhimurium in a one health context: the evolution of a global menace. Sci Total Environ 2023; 896:165203 [View Article] [PubMed]
     [Google Scholar]
  74. Fan J, Cai H, Fang Y, He J, Zhang L et al. Molecular genetic characteristics of plasmid-borne mcr-9 in Salmonella enterica serotype typhimurium and Thompson in Zhejiang, China. Front Microbiol 2022; 13:852434 [View Article] [PubMed]
     [Google Scholar]
  75. Bertelloni F, Cagnoli G, Turchi B, Ebani VV. Low level of colistin resistance and mcr genes presence in Salmonella spp.: evaluation of isolates collected between 2000 and 2020 from animals and environment. Antibiotics 2022; 11:272 [View Article] [PubMed]
     [Google Scholar]
  76. Kieffer N, Royer G, Decousser J-W, Bourrel A-S, Palmieri M et al. mcr-9, an inducible gene encoding an acquired phosphoethanolamine transferase in Escherichia coli, and its origin. Antimicrob Agents Chemother 2019; 63:e00965-19 [View Article] [PubMed]
     [Google Scholar]
  77. Galetti R, Filho RACP, Ferreira JC, Varani AM, Sazinas P et al. The plasmidome of multidrug-resistant emergent Salmonella serovars isolated from poultry. Infect Genet Evol 2021; 89:104716 [View Article] [PubMed]
     [Google Scholar]
  78. Humayoun SB, Hiott LM, Gupta SK, Barrett JB, Woodley TA et al. An assay for determining the susceptibility of Salmonella isolates to commercial and household biocides. PLoS One 2018; 13:e0209072 [View Article] [PubMed]
     [Google Scholar]
  79. Zagui GS, Moreira NC, Santos DV, Darini ALC, Domingo JL et al. High occurrence of heavy metal tolerance genes in bacteria isolated from wastewater: a new concern?. Environ Res 2021; 196:110352 [View Article] [PubMed]
     [Google Scholar]
  80. Kaur I, Purves J, Harwood M, Ketley JM, Andrew PW et al. Role of horizontally transferred copper resistance genes in Staphylococcus aureus and Listeria monocytogenes. Microbiology 2022; 168:001162 [View Article] [PubMed]
     [Google Scholar]
  81. Pierezan MD, Maran BM, Maran EM, Verruck S, Pimentel TC. Chapter six - Relevant safety aspects of raw milk for dairy foods processing. In Toldrá F. eds Advances in Food and Nutrition Research vol 100 Academic Press; 2022 pp 211–264 [View Article]
     [Google Scholar]
  82. Joerger RD, Hanning IB, Ricke SC. Presence of arsenic resistance in Salmonella enterica serovar kentucky and other serovars isolated from poultry. Avian Diseases 2010; 54:1178–1182 [View Article] [PubMed]
     [Google Scholar]
  83. Mourão J, Rebelo A, Ribeiro S, Peixe L, Novais C. Tolerance to arsenic contaminant among multidrug-resistant and copper-tolerant Salmonella successful clones is associated with diverse ars operons and genetic contexts. Environ Microbiol 2020; 22:2829–2842 [View Article] [PubMed]
     [Google Scholar]
  84. Wilson A, Fox EM, Fegan N, Kurtböke DÍ. n.d. Comparative genomics and phenotypic investigations into antibiotic, heavy metal, and disinfectant susceptibilities of Salmonella enterica strains isolated in Australia. Front Microbiol 10: [View Article] [PubMed]
     [Google Scholar]
  85. Argudín MA, Hoefer A, Butaye P. Heavy metal resistance in bacteria from animals. Res Vet Sci 2019; 122:132–147 [View Article] [PubMed]
     [Google Scholar]
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Plasmid-encoded lactose metabolism and mobilized colistin resistance (mcr-9) genes in Salmonella enterica serovars isolated from dairy facilities in the 1980s
M Gen 9, 001149 (2023); https://doi.org/10.1099/mgen.0.001149
/content/journal/mgen/10.1099/mgen.0.001149
/content/journal/mgen/10.1099/mgen.0.001149
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