Emergence of methicillin resistance predates the clinical use of antibiotics.
Animals
Anti-Bacterial Agents
/ history
Arthrodermataceae
/ genetics
Denmark
Europe
Evolution, Molecular
Geographic Mapping
Hedgehogs
/ metabolism
History, 20th Century
Humans
Methicillin Resistance
/ genetics
Methicillin-Resistant Staphylococcus aureus
/ genetics
New Zealand
One Health
Penicillins
/ biosynthesis
Phylogeny
Selection, Genetic
/ genetics
beta-Lactams
/ metabolism
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
12
05
2021
accepted:
18
11
2021
pubmed:
7
1
2022
medline:
11
3
2022
entrez:
6
1
2022
Statut:
ppublish
Résumé
The discovery of antibiotics more than 80 years ago has led to considerable improvements in human and animal health. Although antibiotic resistance in environmental bacteria is ancient, resistance in human pathogens is thought to be a modern phenomenon that is driven by the clinical use of antibiotics
Identifiants
pubmed: 34987223
doi: 10.1038/s41586-021-04265-w
pii: 10.1038/s41586-021-04265-w
pmc: PMC8810379
doi:
Substances chimiques
Anti-Bacterial Agents
0
Penicillins
0
beta-Lactams
0
Types de publication
Historical Article
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
135-141Subventions
Organisme : Medical Research Council
ID : G1001787
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N002660/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/P007201/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S00291X/1
Pays : United Kingdom
Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022. The Author(s).
Références
Davies, J. & Davies, D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417–433 (2010).
pubmed: 20805405
pmcid: 2937522
doi: 10.1128/MMBR.00016-10
European Centre for Disease Prevention and Control, European Medicines Agencies. The Bacterial Challenge: Time to React. A Call to Narrow the Gap Between Multidrug-Resistant Bacteria in the EU and the Development of New Antibacterial Agents https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/0909_TER_The_Bacterial_Challenge_Time_to_React.pdf (2009).
Jevons, M. P. “Celbenin”—resistant Staphylococci. Br. Med. J. 1, 124–125 (1961).
pmcid: 1952888
doi: 10.1136/bmj.1.5219.124-a
Harkins, C. P. et al. Methicillin-resistant Staphylococcus aureus emerged long before the introduction of methicillin into clinical practice. Genome Biol. 18, 130 (2017).
pubmed: 28724393
pmcid: 5517843
doi: 10.1186/s13059-017-1252-9
Chambers, H. F. & DeLeo, F. R. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7, 629–641 (2009).
pubmed: 19680247
pmcid: 2871281
doi: 10.1038/nrmicro2200
Price, L. B. et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3, e00305-11 (2012).
pubmed: 22354957
pmcid: 3280451
doi: 10.1128/mBio.00305-11
Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics http://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf?ua=1 (WHO, 2017).
Rasmussen, S. L. et al. European hedgehogs (Erinaceus europaeus) as a natural reservoir of methicillin-resistant Staphylococcus aureus carrying mecC in Denmark. PLoS ONE 14, e0222031 (2019).
pubmed: 31490992
pmcid: 6730924
doi: 10.1371/journal.pone.0222031
Bengtsson, B. et al. High occurrence of mecC-MRSA in wild hedgehogs (Erinaceus europaeus) in Sweden. Vet. Microbiol. 207, 103–107 (2017).
pubmed: 28757008
doi: 10.1016/j.vetmic.2017.06.004
García-Álvarez, L. et al. Methicillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect. Dis. 11, 595–603 (2011).
pubmed: 21641281
pmcid: 3829197
doi: 10.1016/S1473-3099(11)70126-8
Paterson, G. K., Harrison, E. M. & Holmes, M. A. The emergence of mecC methicillin-resistant Staphylococcus aureus. Trends Microbiol. 22, 42–47 (2014).
pubmed: 24331435
pmcid: 3989053
doi: 10.1016/j.tim.2013.11.003
Marples, M. J. & Smith, J. M. B. The hedgehog as a source of human ringworm. Nature 188, 867–868 (1960).
pubmed: 13767053
doi: 10.1038/188867b0
English, M. P., Evans, C. D., Hewitt, M. & Warin, R. P. “Hedgehog ringworm”. Br. Med. J. 1, 149–151 (1962).
pubmed: 13890287
pmcid: 1957388
doi: 10.1136/bmj.1.5272.149
Smith, J. M. B. & Marples, M. J. A natural reservoir of penicillin-resistant strains of Staphylococcus aureus. Nature 201, 844 (1964).
pubmed: 14161236
doi: 10.1038/201844a0
Smith, J. M. B. & Marples, M. J. Dermatophyte lesions in the hedgehog as a reservoir of penicillin-resistant staphylococci. J. Hyg. 63, 293–303 (1965).
pubmed: 14308356
pmcid: 2134650
doi: 10.1017/S0022172400045174
Smith, J. M. B. Staphylococcus aureus strains associated with the hedgehog Erinaceus europaeus. J. Hyg. Camb. 63, 293–303 (1965).
pubmed: 14308356
pmcid: 2134650
doi: 10.1017/S0022172400045174
Morris, P. & English, M. P. Trichophyton mentagrophytes var. erinacei in British hedgehogs. Sabouraudia 7, 122–128 (1969).
pubmed: 5346186
doi: 10.1080/00362177085190221
Le Barzic, C. et al. Detection and control of dermatophytosis in wild European hedgehogs (Erinaceus europaeus) admitted to a French wildlife rehabilitation centre. J. Fungi 7, 74 (2021).
doi: 10.3390/jof7020074
Dube, F., Söderlund, R., Salomonsson, M. L., Troell, K. & Börjesson, S. Benzylpenicillin-producing Trichophyton erinacei and methicillin resistant Staphylococcus aureus carrying the mecC gene on European hedgehogs: a pilot-study. BMC Microbiol. 21, 212 (2021).
pubmed: 34266385
pmcid: 8283913
doi: 10.1186/s12866-021-02260-9
Hewitt, G. The genetic legacy of the Quaternary ice ages. Nature 405, 907–913 (2000).
pubmed: 10879524
doi: 10.1038/35016000
Brockie, R. E. Distribution and abundance of the hedgehog (Erinaceus europaeus) L. in New Zealand, 1869–1973. N. Z. J. Zool. 2, 445–462 (1975).
doi: 10.1080/03014223.1975.9517886
van den Berg, M. A. et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 26, 1161–1168 (2008).
pubmed: 18820685
doi: 10.1038/nbt.1498
Ullán, R. V., Campoy, S., Casqueiro, J., Fernández, F. J. & Martín, J. F. Deacetylcephalosporin C production in Penicillium chrysogenum by expression of the isopenicillin N epimerization, ring expansion, and acetylation genes. Chem. Biol. 14, 329–339 (2007).
pubmed: 17379148
doi: 10.1016/j.chembiol.2007.01.012
Kitano, K. et al. A novel penicillin produced by strains of the genus Paecilomyces. J. Ferment. Technol. 54, 705–711 (1976).
Petersen, A. et al. Epidemiology of methicillin-resistant Staphylococcus aureus carrying the novel mecC gene in Denmark corroborates a zoonotic reservoir with transmission to humans. Clin. Microbiol. Infect. 19, E16–E22 (2013).
pubmed: 23078039
doi: 10.1111/1469-0691.12036
Richardson, E. J. et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nat. Ecol. Evol. 2, 1468–1478 (2018).
pubmed: 30038246
pmcid: 7610605
doi: 10.1038/s41559-018-0617-0
Holden, M. T. G. et al. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res. 23, 653–664 (2013).
pubmed: 23299977
pmcid: 3613582
doi: 10.1101/gr.147710.112
Strauß, L. et al. Origin, evolution, and global transmission of community-acquired Staphylococcus aureus ST8. Proc. Natl Acad. Sci. USA 114, E10596–E10604 (2017).
pubmed: 29158405
pmcid: 5724248
doi: 10.1073/pnas.1702472114
Nübel, U. et al. Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc. Natl Acad. Sci. USA 105, 14130–14135 (2008).
pubmed: 18772392
pmcid: 2544590
doi: 10.1073/pnas.0804178105
Rasmussen, S. L., Nielsen, J. L., Jones, O. R., Berg, T. B. & Pertoldi, C. Genetic structure of the European hedgehog (Erinaceus europaeus) in Denmark. PLoS ONE 15, e0227205 (2020).
pubmed: 31951621
pmcid: 6968871
doi: 10.1371/journal.pone.0227205
Hansen, J. E. et al. LA-MRSA CC398 in dairy cattle and veal calf farms indicates spillover from pig production. Front. Microbiol. 10, 2733 (2019).
pubmed: 31849885
pmcid: 6887863
doi: 10.3389/fmicb.2019.02733
Eriksson, J. Espinosa-Gongora, C., Stamphøj, I., Larsen, A. R. & Guardabassi, L. Carriage frequency, diversity and methicillin resistance of in Danish small ruminants. Vet. Microbiol. 163, 110–115 (2013).
pubmed: 23290574
doi: 10.1016/j.vetmic.2012.12.006
Danish Integrated Antimicrobial Resistance Monitoring and Research Programme. DANMAP 2019: Use of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria From Food Animals, Food, and Humans in DENMARK https://www.danmap.org/-/media/Sites/danmap/Downloads/Reports/2019/DANMAP_2019.ashx?la=da&hash=AA1939EB449203EF0684440AC1477FFCE2156BA5 (2020).
Veterinary Medicines Directorate. UK Veterinary Antibiotic Resistance and Sales Surveillance Report https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/950126/UK-VARSS_2019_Report__2020-TPaccessible.pdf (2020).
Harrison, E. M. et al. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol. Med. 5, 509–515 (2013).
pubmed: 23526809
pmcid: 3628104
doi: 10.1002/emmm.201202413
Loncaric, I. et al. Characterization of mecC gene-carrying coagulase-negative Staphylococcus spp. isolated from various animals. Vet. Microbiol. 230, 138–144 (2019).
pubmed: 30827379
doi: 10.1016/j.vetmic.2019.02.014
Gómez, P. et al. Detection of MRSA ST3061-t843-mecC and ST398-t011-mecA in white stork nestlings exposed to human residues. J. Antimicrob. Chemother. 71, 53–57 (2016).
pubmed: 26490014
doi: 10.1093/jac/dkv314
Kim, C. et al. Properties of a novel PBP2A protein homolog from Staphylococcus aureus strain LGA251 and its contribution to the β-lactam-resistant phenotype. J. Biol. Chem. 287, 36854–36863 (2012).
pubmed: 22977239
pmcid: 3481288
doi: 10.1074/jbc.M112.395962
Tahlan, K. & Jensen, S. E. Origins of the β-lactam rings in natural products. J. Antibiot. 66, 401–419 (2013).
doi: 10.1038/ja.2013.24
Pantůček, R. et al. Staphylococcus edaphicus sp. nov. isolated in Antarctica harbors the mecC gene and genomic islands with a suspected role in adaptation to extreme environment. Appl. Environ. Microbiol. 84, e01746-17 (2018).
pubmed: 29079617
pmcid: 5752872
doi: 10.1128/AEM.01746-17
D’Costa, V. M., et al. Antibiotic resistance is ancient. Nature 477, 457–461 (2011).
pubmed: 21881561
doi: 10.1038/nature10388
Allen, H. K., Moe, L. A., Rodbumrer, J., Gaarder, A. & Handelsman, J. Functional metagenomics reveals diverse beta-lactamases in a remote Alaskan soil. ISME J. 3, 243–251 (2009).
pubmed: 18843302
doi: 10.1038/ismej.2008.86
Forsberg, K. J. et al. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107–1111 (2012).
pubmed: 22936781
pmcid: 4070369
doi: 10.1126/science.1220761
Forsberg, K. J. et al. Bacterial phylogeny structures soil resistomes across habitats. Nature 509, 612–616 (2014).
pubmed: 24847883
pmcid: 4079543
doi: 10.1038/nature13377
Coll, F. et al. Definition of a genetic relatedness cutoff to exclude recent transmission of meticillin-resistant Staphylococcus aureus: a genomic epidemiology analysis. Lancet Microbe 1, e328–e335 (2020).
pubmed: 33313577
pmcid: 7721685
doi: 10.1016/S2666-5247(20)30149-X
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its application to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
pubmed: 22506599
pmcid: 3342519
doi: 10.1089/cmb.2012.0021
Enright, M. C., Day, N. P., Davies, C. E., Peacock, S. J., Spratt, B. G. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J. Clin. Microbiol. 38, 1008–1015 (2000).
pubmed: 10698988
pmcid: 86325
doi: 10.1128/JCM.38.3.1008-1015.2000
Van Wamel, W. J., Rooijakkers, S. H., Ruyken, M. van Kessel, K. P. & Strijp, J. A. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol. 188, 1310–1315 (2006).
pubmed: 16452413
pmcid: 1367213
doi: 10.1128/JB.188.4.1310-1315.2006
Viana, D. et al. Adaptation of Staphylococcus aureus to ruminant and equine hosts involved SaPI-carried variants of von Willebrand factor-binding protein. Mol. Microbiol. 77, 1583–1594 (2010).
Rooijakkers, S. H. M. et al. Staphylococcal complement inhibitor: structure and active sites. J. Immunol. 179, 2989–2998 (2007).
pubmed: 17709514
doi: 10.4049/jimmunol.179.5.2989
Arndt, D. et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–W21 (2016).
pubmed: 27141966
pmcid: 4987931
doi: 10.1093/nar/gkw387
Bortolaia, V. et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J. Antimicrob. Chemother. 75, 3491–3500 (2020).
pubmed: 32780112
pmcid: 7662176
doi: 10.1093/jac/dkaa345
Clausen, P. T. L. C., Aarestrup, F. M. & Lund, O. Rapid and precise alignment of raw reads against redundant database with KMA. BMC Bioinform. 19, 397 (2018).
doi: 10.1186/s12859-018-2336-6
Sahl, J. W. et al. NASP: an accurate, rapid method for the identification of SNPs in WGS datasets that supports flexible input and output formats. Microb. Genom. 2, e000074 (2016).
pubmed: 28348869
pmcid: 5320593
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrow-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
pubmed: 20644199
pmcid: 2928508
doi: 10.1101/gr.107524.110
DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation sequencing data. Nat. Genet. 43, 491–498 (2011).
pubmed: 21478889
pmcid: 3083463
doi: 10.1038/ng.806
Delcher, A. L., Phillippy, A., Carlton, J. & Salzberg, S. L. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30, 2478–2483 (2002).
pubmed: 12034836
pmcid: 117189
doi: 10.1093/nar/30.11.2478
Kurz, S. et al. Versatile and open software for comparing large genomes. Genome Biol. 5, R12 (2004).
doi: 10.1186/gb-2004-5-2-r12
Guindon, S. & Gasquel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003).
pubmed: 14530136
doi: 10.1080/10635150390235520
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
pubmed: 20525638
doi: 10.1093/sysbio/syq010
Didelot, X. & Wilson, D. J. ClonalFrameML: efficient inference of recombination in whole bacterial genome. PLoS Comput. Biol. 11, e1004041 (2015).
pubmed: 25675341
pmcid: 4326465
doi: 10.1371/journal.pcbi.1004041
Didelot, X. et al. Bayesian inference of ancestral dates on bacterial phylogenetic trees. Nucleic Acids Res. 46, e134 (2018).
pubmed: 30184106
pmcid: 6294524
doi: 10.1093/nar/gky783
Didelot, X., Siveroni, I. & Volz, E. M. Additive uncorrelated relaxed clock models for the dating of genomic epidemiology phylogenies. Mol. Biol. Evol. 38, 307–317 (2021).
pubmed: 32722797
doi: 10.1093/molbev/msaa193
Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006).
Volz, E. M. & Frost, S. D. Scalable relaxed clock phylogenetic dating. Virus Evol. 3, vex025 (2017).
doi: 10.1093/ve/vex025
Wang, M. et al. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat. Biotechnol. 34, 828–837 (2016).
pubmed: 27504778
pmcid: 5321674
doi: 10.1038/nbt.3597
Adusumilli, R. & Mallick, P. Data conversion with ProteoWizard msConvert. Methods Mol. Biol. 1550, 339–368 (2017).
pubmed: 28188540
doi: 10.1007/978-1-4939-6747-6_23