Frequent convergence of mcr-9 and carbapenemase genes in Enterobacter cloacae complex driven by epidemic plasmids and host incompatibility

References

• Giamarellou H, Poulakou G. Multidrug-Resistant gram-negative infections. Drugs. 2009;69:1879–1901.
   PubMed Web of Science ®Google Scholar
• van Duin D, Doi Y. Commentary: Outbreak of colistin-resistant, carbapenemase-producing klebsiella pneumoniae: Are We at the End of the road? J Clin Microbiol. 2015;53:3116–3117.
   PubMed Web of Science ®Google Scholar
• D'Onofrio V, Conzemius R, Varda-Brkic D, et al. Epidemiology of colistin-resistant, carbapenemase-producing enterobacteriaceae and acinetobacter baumannii in Croatia. Infect Genet Evol. 2020;81:104263.
   PubMed Web of Science ®Google Scholar
• Kieffer N, Ahmed MO, Elramalli AK, et al. Colistin-resistant carbapenemase-producing isolates among klebsiella spp. and acinetobacter baumannii in Tripoli, Libya. J Glob Antimicrob Resist. 2018;13:37–39.
   PubMed Web of Science ®Google Scholar
• Liu Y-Y, Wang Y, Walsh TR, 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.
   PubMed Web of Science ®Google Scholar
• Xavier BB, Lammens C, Ruhal R, et al. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Eurosurveillance. 2016;21:pii = 30280.
   Web of Science ®Google Scholar
• AbuOun M, Stubberfield EJ, Duggett NA, et al. mcr-1 and mcr-2 (mcr-6.1) variant genes identified in moraxella species isolated from pigs in Great Britain from 2014 to 2015. J Antimicrob Chemother. 2017;72:2745–2749.
   PubMed Web of Science ®Google Scholar
• Borowiak M, Fischer J, Hammerl JA, et al. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting salmonella enterica subsp. enterica serovar paratyphi B. J Antimicrob Chemother. 2017;72:3317–3324.
   PubMed Web of Science ®Google Scholar
• Carattoli A, Villa L, Feudi C, et al. Novel plasmid-mediated colistin resistance mcr-4 gene in salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Eurosurveillance. 2017;22:pii = 30589.
   Web of Science ®Google Scholar
• Yin W, Li H, Shen Y, et al. Effects of a bio-invasion of the pacific oyster, crassostrea gigas (thunberg, 1793) in five shallow water habitats in scandinavia. mBio. 2017;8:543–00517.
   PubMed Web of Science ®Google Scholar
• Wang X, Wang Y, Zhou Y, et al. Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing klebsiella pneumoniae. Emerg Microbes Infec. 2018;7:122.
   PubMed Web of Science ®Google Scholar
• Yang YQ, Li YX, Lei CW, et al. Novel plasmid-mediated colistin resistance gene mcr-7.1 in klebsiella pneumoniae. J Antimicrob Chemother. 2018;73:1791–1795.
   PubMed Web of Science ®Google Scholar
• Carroll LM, Gaballa A, Guldimann C, et al. Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible salmonella enterica serotype typhimurium isolate. mBio. 2019;10:e00853–e00819.
   PubMed Web of Science ®Google Scholar
• Wang C, Feng Y, Liu L, et al. Identification of novel mobile colistin resistance gene mcr-10. Emerg Microbes Infect. 2020;9:508–516.
   PubMed Web of Science ®Google Scholar
• Ma S, Sun C, Hulth A, et al. Mobile colistin resistance gene mcr-5 in porcine aeromonas hydrophila. J Antimicrob Chemother. 2018;73:1777–1780.
   PubMed Web of Science ®Google Scholar
• Xu T, Zhang C, Ji Y, et al. Identification of mcr-10 carried by self-transmissible plasmids and chromosome in Enterobacter roggenkampii strains isolated from hospital sewage water. Environ Pollut. 2021;268:115706.
   PubMed Web of Science ®Google Scholar
• Macesic N, Blakeway LV, Stewart JD, et al. Silent spread of mobile colistin resistance gene mcr-9.1 on IncHI2 ‘superplasmids’ in clinical carbapenem-resistant enterobacterales. Clin Microbiol Infect. 2021;27:1856.1856.e7–1856.e13.
   Web of Science ®Google Scholar
• Ling Z, Yin W, Shen Z, et al. Epidemiology of mobile colistin resistance genes mcr-1 to mcr-9. J Antimicrob Chemother. 2020;75:3087–3095.
   PubMed Web of Science ®Google Scholar
• Alba P, Leekitcharoenphon P, Franco A, et al. Molecular epidemiology of mcr-encoded colistin resistance in enterobacteriaceae from food-producing animals in Italy revealed through the EU harmonized antimicrobial resistance monitoring. Front Microbiol. 2018;9:1217.
   PubMed Web of Science ®Google Scholar
• Jiang Y, Zhang Y, Lu J, et al. Clinical relevance and plasmid dynamics of mcr-1-positive Escherichia coli in China: a multicentre case-control and molecular epidemiological study. The Lancet Microbe. 2020;1:e24–e33.
   PubMedGoogle Scholar
• Nesporova K, Jamborova I, Valcek A, et al. Various conjugative plasmids carrying the mcr-5 gene in Escherichia coli isolates from healthy chickens in Paraguay. J Antimicrob Chemother. 2019;74:3394–3397.
   PubMed Web of Science ®Google Scholar
• Chavda KD, Westblade LF, Satlin MJ, et al. First report of blaVIM-4- and mcr-9-coharboring enterobacter species isolated from a pediatric patient. mSphere. 2019;4:e00629–e00619.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Li Y, Wang G, et al. Coproduction of MCR-9 and NDM-1 by colistin-resistant Enterobacter hormaechei isolated from bloodstream infection. Infect Drug Resist. 2019;Volume 12:2979–2985.
   Web of Science ®Google Scholar
• Davin-Regli A, Lavigne JP, Pages JM. Enterobacter spp.: Update on Taxonomy, Clinical Aspects, and Emerging Antimicrobial ResistanceEnterobacter spp.: update on taxonomy, clinical aspects, and emerging antimicrobial resistance. Clin Microbiol Rev. 2019;32:e00002–19.
   PubMed Web of Science ®Google Scholar
• Sutton GG, Brinkac LM, Clarke TH, et al. Enterobacter hormaechei subsp. hoffmannii subsp. nov., Enterobacter hormaechei subsp. xiangfangensis comb. nov., Enterobacter roggenkampii sp. nov., and Enterobacter muelleri is a later heterotypic synonym of Enterobacter asburiae based on computational analysis of sequenced Enterobacter genomes. F1000Res. 2018;7:521.
   PubMedGoogle Scholar
• Chavda KD, Chen L, Fouts DE, et al. Enterobacter spp.: New Insights into Phylogeny, Population Structure, and Resistance MechanismsComprehensive genome analysis of carbapenemase-producing Enterobacter spp.: new insights into phylogeny, population structure, and resistance mechanisms. mBio. 2016;7:e02093–e02016.
   PubMed Web of Science ®Google Scholar
• Mediavilla JR, Patrawalla A, Chen L, et al. Colistin- and carbapenem-resistant Escherichia coli harboring mcr-1 and blaNDM-5, causing a complicated Urinary Tract Infection in a patient from the United States. mBio. 2016;7:e01191–e01116.
   PubMed Web of Science ®Google Scholar
• Yao X, Doi Y, Zeng L, et al. Carbapenem-resistant and colistin-resistant Escherichia coli co-producing NDM-9 and MCR-1. Lancet Infect Dis. 2016;16:288–289.
   PubMed Web of Science ®Google Scholar
• Khalifa HO, Soliman AM, Saito T, et al. First report of blaVIM-1-, blaNDM-1-, and mcr-9-co-harboring foodborne klebsiella pneumoniae. Antimicrob Agents Chemother. 2020;64:e00882–e00820.
   PubMed Web of Science ®Google Scholar
• Sun L, Zhao X, Wang L, et al. Coexistence of mcr-9 and blaNDM-1 in a multidrug-resistant Enterobacter hormaechei strain recovered from a bloodstream infection in China. J Glob Antimicrob Resist. 2021;24:440–442.
   PubMed Web of Science ®Google Scholar
• Simoni S, Mingoia M, Brenciani A, et al. First inchi2 plasmid carrying mcr-9.1, blaVIM-1, and double copies of blaKPC-3 in a multidrug-resistant Escherichia coli human isolate. mSphere. 2021;6:e0030221.
   PubMed Web of Science ®Google Scholar
• Chen W, Hu Z, Wang S, et al. Letter to the Editor: Characterization of a clinical Enterobacter hormaechei strain belonging to epidemic clone ST418 co-carrying blaNDM-1, blaIMP-4 and mcr-9.1. Microb Drug Resist. 2022;28:180–184.
   PubMed Web of Science ®Google Scholar
• Liao W, Cui Y, Quan J, et al. High prevalence of colistin resistance and mcr-9/10 genes in Enterobacter spp. in a tertiary hospital over a decade. Int J Antimicrob Agents. 2022;106573.
   PubMed Web of Science ®Google Scholar
• Ji Y, Wang P, Xu T, et al. Development of a one-step multiplex PCR assay for differential detection of four species (Enterobacter cloacae, Enterobacter hormaechei, Enterobacter roggenkampii, and Enterobacter kobei) belonging to Enterobacter cloacae complex with clinical significance. Front Cell Infect Mi. 2021;11:677089.
   PubMed Web of Science ®Google Scholar
• Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120.
   PubMed Web of Science ®Google Scholar
• Bankevich A, Nurk S, Antipov D, et al. Spades: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–477.
   PubMed Web of Science ®Google Scholar
• Foong J, Girdea M, Stavropoulos J, et al. Prioritizing clinically relevant copy number variation from genetic interactions and gene function data. PLoS One. 2015;10:e0139656.
   PubMed Web of Science ®Google Scholar
• Hunt M, Silva ND, Otto TD, et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol. 2015;16:294.
   PubMed Web of Science ®Google Scholar
• Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–2069.
   PubMed Web of Science ®Google Scholar
• Zankari E, Hasman H, Cosentino S, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67:2640–2644.
   PubMed Web of Science ®Google Scholar
• Carattoli A, Zankari E, García-Fernández A, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58:3895–3903.
   PubMed Web of Science ®Google Scholar
• Richter M, Rossello-Mora R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 2009;106:19126–19131.
   PubMed Web of Science ®Google Scholar
• Treangen TJ, Ondov BD, Koren S, et al. The harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 2014;15:524.
   PubMed Web of Science ®Google Scholar
• Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011;27:1009–1010.
   PubMed Web of Science ®Google Scholar
• Alikhan NF, Petty NK, Ben Zakour NL, et al. BLAST ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12: 402.
   PubMed Web of Science ®Google Scholar
• Camacho C, Coulouris G, Avagyan V, et al. Blast+: architecture and applications. BMC Bioinformatics. 2009;10:421.
   PubMed Web of Science ®Google Scholar
• Gao H, Liu Y, Wang R, et al. The transferability and evolution of NDM-1 and KPC-2 co-producing klebsiella pneumoniae from clinical settings. EBioMedicine. 2020;51:102599.
   PubMed Web of Science ®Google Scholar
• Xu T, Xue C-X, Huang J, et al. Emergence of an epidemic hypervirulent clone of Enterobacter hormaechei coproducing MCR-9 and carbapenemases. The Lancet Microbe. 2022;3:e474–e475.
   PubMedGoogle Scholar
• Nakamura A, Nakamura T, Niki M, et al. Genomic characterization of ESBL- and carbapenemase-positive enterobacteriaceae co-harboring mcr-9 in Japan. Front Microbiol. 2021;12:665432.
   PubMed Web of Science ®Google Scholar
• Khedher MB, Baron SA, Riziki T, et al. Massive analysis of 64,628 bacterial genomes to decipher water reservoir and origin of mobile colistin resistance genes: is there another role for these enzymes? Sci Rep. 2020;10:5970.
   PubMed Web of Science ®Google Scholar
• Sato T, Usui M, Harada K, et al. Complete genome sequence of an mcr-10-possessing Enterobacter roggenkampii strain isolated from a dog in Japan. Microbiol Resour Announc. 2021;10:e0042621.
   PubMed Web of Science ®Google Scholar
• Guan J, Li L, Zheng LA-O, et al. First report of the colistin resistance gene mcr-10.1 carried by Inc(pA1763-KPC) plasmid pSL12517-mcr10.1 in Enterobacter cloacae in Sierra Leone. Microbiol Spectr. 2022;e0112722. Online ahead of print.
   PubMed Web of Science ®Google Scholar
• Mezzatesta ML, Gona F, Stefani S. Enterobacter cloacae complex: clinical impact and emerging antibiotic resistance. Future Microbiol. 2012;7:887–902.
   PubMed Web of Science ®Google Scholar
• Zhou K, Yu W, Cao X, et al. Characterization of the population structure, drug resistance mechanisms and plasmids of the community-associated Enterobacter cloacae complex in China. J Antimicrob Chemother. 2018;73:66–76.
   PubMed Web of Science ®Google Scholar
• Tyson GH, Li C, Hsu CH, et al. The mcr-9 gene of Salmonella and E. coli is not associated with colistin resistance in the United States. Antimicrob Agents Chemother. 2020;64:e00573–e00520.
   PubMed Web of Science ®Google Scholar
• Borjesson S, Greko C, Myrenas M, et al. A link between the newly described colistin resistance gene mcr-9 and clinical enterobacteriaceae isolates carrying blaSHV-12 from horses in Sweden. J Glob Antimicrob Resist. 2020;20:285–289.
   PubMed Web of Science ®Google Scholar
• Li Y, Dai X, Zeng J, et al. Characterization of the global distribution and diversified plasmid reservoirs of the colistin resistance gene mcr-9. Sci Rep. 2020;10:8113.
   PubMed Web of Science ®Google Scholar
• Chen J, Tian S, Nian H, et al. Carbapenem-resistant Enterobacter cloacae complex in a tertiary hospital in northeast China, 2010-2019. BMC Infect Dis 2021;21:611.
   PubMed Web of Science ®Google Scholar
• Jin C, Zhang J, Wang Q, et al. Molecular characterization of carbapenem-resistant Enterobacter cloacae in 11 Chinese cities. Front Microbiol. 2018;9:1597.
   PubMed Web of Science ®Google Scholar