Antibiotic resistance plasmid composition and architecture in Escherichia coli isolates from meat.
Animals
Anti-Bacterial Agents
/ pharmacology
Drug Resistance, Multiple, Bacterial
/ genetics
Escherichia coli
/ drug effects
Escherichia coli Infections
/ microbiology
Gene Order
Gene Transfer, Horizontal
/ genetics
High-Throughput Nucleotide Sequencing
/ methods
Humans
Meat
/ microbiology
Multigene Family
/ genetics
Plasmids
/ classification
Replicon
/ genetics
Tetracycline Resistance
/ genetics
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
22 01 2021
22 01 2021
Historique:
received:
28
10
2020
accepted:
08
01
2021
entrez:
23
1
2021
pubmed:
24
1
2021
medline:
21
9
2021
Statut:
epublish
Résumé
Resistance plasmids play a crucial role in the transfer of antimicrobial resistance from the veterinary sector to human healthcare. In this study plasmids from foodborne Escherichia coli isolates with a known (ES)BL or tetracycline resistance were sequenced entirely with short- and long-read technologies to obtain insight into their composition and to identify driving factors for spreading. Resistant foodborne E. coli isolates often contained several plasmids coding for resistance to various antimicrobials. Most plasmids were large and contained multiple resistance genes in addition to the selected resistance gene. The majority of plasmids belonged to the IncI, IncF and IncX incompatibility groups. Conserved and variable regions could be distinguished in each of the plasmid groups. Clusters containing resistance genes were located in the variable regions. Tetracycline and (extended spectrum) beta-lactamase resistance genes were each situated in separate clusters, but sulphonamide, macrolide and aminoglycoside formed one cluster and lincosamide and aminoglycoside another. In most plasmids, addiction systems were found to maintain presence in the cell.
Identifiants
pubmed: 33483623
doi: 10.1038/s41598-021-81683-w
pii: 10.1038/s41598-021-81683-w
pmc: PMC7822866
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2136Références
Carattoli, A. Plasmids and the spread of resistance. Int. J. Med. Microbiol. 303, 298–304 (2013).
pubmed: 23499304
doi: 10.1016/j.ijmm.2013.02.001
Levy, S. B. & Marshall, B. Antibacterial resistance worldwide: Causes, challenges and responses. Nat. Med. 10, S122–S129 (2004).
pubmed: 15577930
doi: 10.1038/nm1145
Lopatkin, A. J. et al. Persistence and reversal of plasmid-mediated antibiotic resistance. Nat. Commun. 8, 1689 (2017).
pubmed: 29162798
pmcid: 5698434
doi: 10.1038/s41467-017-01532-1
Sommer, M. O. A., Munck, C., Toft-Kehler, R. V. & Andersson, D. I. Prediction of antibiotic resistance: Time for a new preclinical paradigm?. Nat. Rev. Microbiol. 15, 689–696 (2017).
pubmed: 28757648
doi: 10.1038/nrmicro.2017.75
Dionisio, F., Matic, I., Radman, M., Rodrigues, O. R. & Taddei, F. Plasmids spread very fast in heterogeneous bacterial communities. Genetics 162, 1525–1532 (2002).
pubmed: 12524329
pmcid: 1462386
doi: 10.1093/genetics/162.4.1525
Threlfall, E. J., Ward, L. R., Frost, L. S. & Willshaw, G. A. The emergence and spread of antibiotic resistance in food-borne bacteria. Int. J. Food Microbiol. 62, 1–5 (2000).
pubmed: 11139009
doi: 10.1016/S0168-1605(00)00351-2
Tacconelli, E. et al. Discovery, research, and development of new antibiotics: The WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet. Infect. Dis 18, 318–327 (2018).
pubmed: 29276051
doi: 10.1016/S1473-3099(17)30753-3
Verraes, C. et al. Antimicrobial resistance in the food chain: A review. Int. J. Environ. Res. Public Health 10, 2643–2669 (2013).
pubmed: 23812024
pmcid: 3734448
doi: 10.3390/ijerph10072643
Stine, O. C. et al. Widespread distribution of tetracycline resistance genes in a confined animal feeding facility. Int. J. Antimicrob. Agents 29, 348–352 (2007).
pubmed: 17287111
doi: 10.1016/j.ijantimicag.2006.11.015
Kaesbohrer, A. et al. Diversity in prevalence and characteristics of ESBL/pAmpC producing E. coli in food in Germany. Vet. Microbiol. 233, 52–60 (2019).
pubmed: 31176413
doi: 10.1016/j.vetmic.2019.03.025
Dierikx, C. et al. Extended-spectrum-beta-lactamase- and AmpC-beta-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J. Antimicrob. Chemother. 68, 60–67 (2013).
pubmed: 22949623
doi: 10.1093/jac/dks349
Fischer, J. et al. Simultaneous occurrence of MRSA and ESBL-producing Enterobacteriaceae on pig farms and in nasal and stool samples from farmers. Vet. Microbiol. 200, 107–113 (2017).
pubmed: 27328620
doi: 10.1016/j.vetmic.2016.05.021
Mughini-Gras, L. et al. Attributable sources of community-acquired carriage of Escherichia coli containing β-lactam antibiotic resistance genes: A population-based modelling study. Lancet Planet. Health 3, e357–e369 (2019).
pubmed: 31439317
doi: 10.1016/S2542-5196(19)30130-5
CDC. 2020. Antibiotic Resistance, Food, and Food Animals. https://www.cdc.gov/foodsafety/challenges/antibiotic-resistance.html . (Accessed 29 July 2020).
Couturier, M., Bex, F., Bergquist, P. L. & Maas, W. K. Identification and classification of bacterial plasmids. Microbiol. Rev. 52, 375–395 (1988).
pubmed: 3054468
pmcid: 373151
doi: 10.1128/mr.52.3.375-395.1988
Thomas, C. M. Plasmid incompatibility. Mol. Life Sci. https://doi.org/10.1007/978-1-4614-6436-5_565-2 (2014).
doi: 10.1007/978-1-4614-6436-5_565-2
Brolund, A. Overview of ESBL-producing Enterobacteriaceae from a Nordic perspective. Infect. Ecol. Epidemiol. 4, 10.3402/iee.v4.24555. https://doi.org/10.3402/iee.v4.24555 (2014).
Orlek, A. et al. Plasmid classification in an era of whole-genome sequencing: Application in studies of antibiotic resistance epidemiology. Front. Microbiol. 8, 182 (2017).
pubmed: 28232822
pmcid: 5299020
doi: 10.3389/fmicb.2017.00182
Fernandez-Lopez, R., de Toro, M., Moncalian, G., Garcillan-Barcia, M. P. & de la Cruz, F. Comparative genomics of the conjugation region of f-like plasmids: five shades of F. Front. Mol. Biosci. 3, 71 (2016).
pubmed: 27891505
pmcid: 5102898
doi: 10.3389/fmolb.2016.00071
Zhang, D. et al. Replicon-based typing of inci-complex plasmids, and comparative genomics analysis of incigamma/K1 plasmids. Front. Microbiol. 10, 48 (2019).
pubmed: 30761100
pmcid: 6361801
doi: 10.3389/fmicb.2019.00048
Arutyunov, D. & Frost, L. S. F conjugation: Back to the beginning. Plasmid 70, 18–32 (2013).
pubmed: 23632276
doi: 10.1016/j.plasmid.2013.03.010
Llosa, M., Gomis-Rüth, F. X., Coll, M. & de la Cruz, F. Bacterial conjugation: A two-step mechanism for DNA transport. Mol. Microbiol. 45, 1–8 (2002).
pubmed: 12100543
doi: 10.1046/j.1365-2958.2002.03014.x
Schroder, G. & Lanka, E. The mating pair formation system of conjugative plasmids-A versatile secretion machinery for transfer of proteins and DNA. Plasmid 54, 1–25 (2005).
pubmed: 15907535
doi: 10.1016/j.plasmid.2005.02.001
Unterholzner, S. J., Poppenberger, B. & Rozhon, W. Toxin-antitoxin systems: Biology, identification, and application. Mob. Genet. Elements 3, e26219 (2013).
pubmed: 24251069
pmcid: 3827094
doi: 10.4161/mge.26219
Zielenkiewicz, U. & Ceglowski, P. Mechanisms of plasmid stable maintenance with special focus on plasmid addiction systems. Acta Biochim. Pol. 48, 1003–1023 (2001).
pubmed: 11995964
doi: 10.18388/abp.2001_3863
van Hoek, A. H. et al. Acquired antibiotic resistance genes: An overview. Front. Microbiol. 2, 203 (2011).
pubmed: 22046172
pmcid: 3202223
Del Castillo, C. S. et al. Comparative sequence analysis of a multidrug-resistant plasmid from Aeromonas hydrophila. Antimicrob. Agents Chemother. 57, 120–129 (2013).
pubmed: 23070174
pmcid: 3535917
doi: 10.1128/AAC.01239-12
Bennett, P. M. Plasmid encoded antibiotic resistance: Acquisition and transfer of antibiotic resistance genes in bacteria. Br. J. Pharmacol. 153(Suppl 1), S347–S357 (2008).
pubmed: 18193080
pmcid: 2268074
doi: 10.1038/sj.bjp.0707607
Stokes, H. W. & Gillings, M. R. Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol. Rev. 35, 790–819 (2011).
pubmed: 21517914
doi: 10.1111/j.1574-6976.2011.00273.x
Costa, T. R. D. et al. Structure of the bacterial sex F pilus reveals an assembly of a stoichiometric protein-phospholipid complex. Cell 166(1436–1444), e10 (2016).
Bonnet, R. Growing group of extended-spectrum beta-lactamases: The CTX-M enzymes. Antimicrob. Agents Chemother. 48, 1–14 (2004).
pubmed: 14693512
pmcid: 310187
doi: 10.1128/AAC.48.1.1-14.2004
Canton, R., Gonzalez-Alba, J. M. & Galan, J. C. CTX-M enzymes: Origin and diffusion. Front. Microbiol. 3, 110 (2012).
pubmed: 22485109
pmcid: 3316993
doi: 10.3389/fmicb.2012.00110
Falgenhauer, L. et al. Colistin resistance gene mcr-1 in extended-spectrum β-lactamase-producing and carbapenemase-producing Gram-negative bacteria in Germany. Lancet. Infect. Dis. 16, 282–283 (2016).
pubmed: 26774242
doi: 10.1016/S1473-3099(16)00009-8
Lo, W. U. et al. Highly conjugative IncX4 plasmids carrying blaCTX-M in Escherichia coli from humans and food animals. J. Med. Microbiol. 63, 835–840 (2014).
pubmed: 24595536
doi: 10.1099/jmm.0.074021-0
Moritz, E. M. & Hergenrother, P. J. Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycin-resistant enterococci. Proc. Natl. Acad. Sci. USA 104, 311–316 (2007).
pubmed: 17190821
doi: 10.1073/pnas.0601168104
Williams, J. J., Halvorsen, E. M., Dwyer, E. M., DiFazio, R. M. & Hergenrother, P. J. Toxin-antitoxin (TA) systems are prevalent and transcribed in clinical isolates of Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 322, 41–50 (2011).
pubmed: 21658105
doi: 10.1111/j.1574-6968.2011.02330.x
Rozwandowicz, M. et al. Plasmids carrying antimicrobial resistance genes in Enterobacteriaceae. J. Antimicrob. Chemother. 73, 1121–1137 (2018).
pubmed: 29370371
doi: 10.1093/jac/dkx488
Partridge, S. R., Kwong, S. M., Firth, N. & Jensen, S. O. Mobile genetic elements associated with antimicrobial resistance. Clin. Microbiol. Rev. 31, 1–61 (2018).
doi: 10.1128/CMR.00088-17
Shintani, M., Sanchez, Z. K. & Kimbara, K. Genomics of microbial plasmids: Classification and identification based on replication and transfer systems and host taxonomy. Front. Microbiol. 6, 242 (2015).
pubmed: 25873913
pmcid: 4379921
doi: 10.3389/fmicb.2015.00242
Austin, S. & Nordström, K. Partition-mediated incompatibility of bacterial plasmids. Cell 60, 351–354 (1990).
pubmed: 2406018
doi: 10.1016/0092-8674(90)90584-2
Ebersbach, G., Sherratt, D. J. & Gerdes, K. Partition-associated incompatibility caused by random assortment of pure plasmid clusters. Mol. Microbiol. 56, 1430–1440 (2005).
pubmed: 15916596
doi: 10.1111/j.1365-2958.2005.04643.x
Novick, R. P. Plasmid incompatibility. Microbiol. Rev. 51, 381–395 (1987).
pubmed: 3325793
pmcid: 373122
doi: 10.1128/mr.51.4.381-395.1987
Sykora, P. Macroevolution of plasmids: A model for plasmid speciation. J. Theor. Biol. 159, 53–65 (1992).
pubmed: 1291811
doi: 10.1016/S0022-5193(05)80767-2
von Wintersdorff, C. J. et al. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front. Microbiol. 7, 173 (2016).
Poirel, L., Decousser, J. W. & Nordmann, P. Insertion sequence ISEcp1B is involved in expression and mobilization of a bla(CTX-M) beta-lactamase gene. Antimicrob. Agents Chemother. 47, 2938–2945 (2003).
pubmed: 12936998
pmcid: 182628
doi: 10.1128/AAC.47.9.2938-2945.2003
Pal, C., Bengtsson-Palme, J., Kristiansson, E. & Larsson, D. G. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genom. 16, 964 (2015).
doi: 10.1186/s12864-015-2153-5
Sota, M. et al. Region-specific insertion of transposons in combination with selection for high plasmid transferability and stability accounts for the structural similarity of IncP-1 plasmids. J. Bacteriol. 189, 3091–3098 (2007).
pubmed: 17277066
pmcid: 1855856
doi: 10.1128/JB.01906-06
Partridge, S. R. Analysis of antibiotic resistance regions in Gram-negative bacteria. FEMS Microbiol. Rev. 35, 820–855 (2011).
pubmed: 21564142
doi: 10.1111/j.1574-6976.2011.00277.x
Tauch, A., Götker, S., Pühler, A., Kalinowksi, J. & Thierbach, G. The 27.8-kb R-plasmid pTET3 from Corynebacterium glutamicum encodes the aminoglycoside adenyltransferase gene cassette aadA9 and the regulated tetracycline efflux system Tet 33 flanked by active copies of the widespread insertion sequence IS6100. Plasmid 48, 117–129 (2002).
pubmed: 12383729
doi: 10.1016/S0147-619X(02)00120-8
Lafond, M., Couture, F., Vézina, G. & Levesque, R. C. Evolutionary perspectives on multiresistance b-lactanase transposons. J. Bacteriol. 171, 6423–6429 (1989).
pubmed: 2556363
pmcid: 210530
doi: 10.1128/jb.171.12.6423-6429.1989
Seiffert, S. N. et al. Plasmids carrying blaCMY-2/4 in Escherichia coli from poultry, poultry meat, and humans belong to a novel IncK subgroup designated IncK2. Front. Microbiol. 8, 407 (2017).
pubmed: 28360894
pmcid: 5350095
doi: 10.3389/fmicb.2017.00407
Yamamoto, T., Yamagata, S., Horii, K. & Yamagishi, S. Comparison of transcription of b-lactamase genes specified by various ampicillin transposons. J. Bacteriol. 150, 269–276 (1982).
pubmed: 6277863
pmcid: 220109
doi: 10.1128/jb.150.1.269-276.1982
Carattoli, A. Resistance plasmid families in Enterobacteriaceae. Antimicrob. Agents Chemother. 53, 2227–2238 (2009).
pubmed: 19307361
pmcid: 2687249
doi: 10.1128/AAC.01707-08
Handel, N., Otte, S., Jonker, M., Brul, S. & ter Kuile, B. H. Factors that affect transfer of the IncI1 beta-lactam resistance plasmid pESBL-283 between E. coli strains. PLoS ONE 10, e0123039 (2015).
pubmed: 25830294
pmcid: 4382111
doi: 10.1371/journal.pone.0123039
Schuurmans, J. M. et al. Effect of growth rate and selection pressure on rates of transfer of an antibiotic resistance plasmid between E. coli strains. Plasmid 72, 1–8 (2014).
pubmed: 24525238
doi: 10.1016/j.plasmid.2014.01.002
Hoeksema, M., Jonker, M. J., Brul, S. & Ter Kuile, B. H. Effects of a previously selected antibiotic resistance on mutations acquired during development of a second resistance in Escherichia coli. BMC Genom. 20, 284 (2019).
doi: 10.1186/s12864-019-5648-7
Tsang, J. Bacterial plasmid addiction systems and their implications for antibiotic drug development. Postdoc J. 5, 3–9 (2017).
pubmed: 28781980
pmcid: 5542005
Jo, S. J. & Woo, G. J. Molecular characterization of plasmids encoding CTX-M beta-lactamases and their associated addiction systems circulating among Escherichia coli from retail chickens, chicken farms, and slaughterhouses in Korea. J. Microbiol. Biotechnol. 26, 270–276 (2016).
pubmed: 26562691
doi: 10.4014/jmb.1507.07048
Makarova, K. S., Wolf, Y. I. & Koonin, E. V. Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct. 4, 19 (2009).
pubmed: 19493340
pmcid: 2701414
doi: 10.1186/1745-6150-4-19
National Institute for Public Health and the Environment. 2020. Nethmap-Maran 2020. The Netherlands.
Schuurmans, J. M., Nuri Hayali, A. S., Koenders, B. B. & ter Kuile, B. H. Variations in MIC value caused by differences in experimental protocol. J. Microbiol. Methods 79(1), 44–47. https://doi.org/10.1016/j.mimet.2009.07.017 (2009).
doi: 10.1016/j.mimet.2009.07.017
pubmed: 19635505
Garcia-Fernandez, A., Fortini, D., Veldman, K., Mevius, D. & Carattoli, A. Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J. Antimicrob. Chemother. 63, 274–281 (2009).
pubmed: 19001452
doi: 10.1093/jac/dkn470
Jackman, S. D. et al. ABySS 2.0: Resource-efficient assembly of large genomes using a Bloom filter. Genome Res. 27, 768–777 (2017).
pubmed: 28232478
pmcid: 5411771
doi: 10.1101/gr.214346.116
Chaisson, M.J., Tesler, G. Mapping single molecule sequencing reads using basic local alignment with succesive refinement (BLASR): Application and theory. BMC Bioinform. 13, 238. https://doi.org/10.1186/1471-2105-13-238 (2012).
Boetzer, M. & Pirovano, W. SSPACE-LongRead: Scaffolding bacterial draft genomes using long read sequence information. BMC Bioinform. 15, 211 (2014).
doi: 10.1186/1471-2105-15-211
Boetzer, M. & Pirovano, W. Toward almost closed genomes with GapFiller. Genome Biol. 13, 1–9 (2012).
doi: 10.1186/gb-2012-13-6-r56
Walker, B. J. et al. Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963 (2014).
pubmed: 25409509
pmcid: 4237348
doi: 10.1371/journal.pone.0112963
Margos, G. et al. Lost in plasmids: Next generation sequencing and the complex genome of the tick-borne pathogen Borrelia burgdorferi. BMC Genom. 18, 422 (2017).
doi: 10.1186/s12864-017-3804-5
Brandt, C. et al. Assessing genetic diversity and similarity of 435 KPC-carrying plasmids. Sci. Rep. 9, 11223 (2019).
pubmed: 31375735
pmcid: 6677891
doi: 10.1038/s41598-019-47758-5
Bortolaia, V. et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J. Antimicrob. Chemother. https://doi.org/10.1093/jac/dkaa345 (2020).
doi: 10.1093/jac/dkaa345
pubmed: 32780112
pmcid: 7729385
Carattoli, A. et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895–3903 (2014).
pubmed: 24777092
pmcid: 4068535
doi: 10.1128/AAC.02412-14
Aziz, R. K. et al. The RAST Server: Rapid annotations using subsystems technology. BMC Genom. 9, 75 (2008).
doi: 10.1186/1471-2164-9-75
Alikhan, N. F., Petty, N. K., Ben Zakour, N. L. & Beatson, S. A. BLAST Ring Image Generator (BRIG): Simple prokaryote genome comparisons. BMC Genom. 12, 402 (2011).
doi: 10.1186/1471-2164-12-402